|

Received: 10 May 2016    Accepted: 23 November 2016

DOI: 10.1111/anu.12532

REVIEW

Dietary effects of soybean products on gut microbiota and

immunity of aquatic animals: A review

Z. Zhou1 | E. Ringø2 | R.E. Olsen3,4 | S.K. Song5

1
Key Laboratory for Feed Biotechnology of
the Ministry of Agriculture, Feed Research Abstract
Institute, Chinese Academy of Agricultural Soybean meal (SBM) is one of the most commonly used vegetable ingredient to re-
Sciences, Beijing, China
2
place fish meal in fish diets. However, SBM is limiting in some essential amino acids
Norwegian College of Fishery
Science, Faculty of Biosciences, Fisheries and contains numerous antinutritional factors and antigens that can affect intestinal
and Economics, UiT The Arctic University of
microbiota and innate immune system in several finfish species and crustaceans and
Norway, Tromsø, Norway
3 compromise health. The impact of SBM on health and gut microbiota of aquatic ani-
Institute of Biology, Norwegian University of
Science and Technology, Trondheim, Norway mals is not only affected by SBM in general, but also on the degree of treatment of the
4
Matre Research Station, Institute of Marine meal and exposure. Recently, many studies are actively seeking ways to complement
Research, Matredal, Norway
5
or balance those adverse responses induced by high inclusion of SBM in aquaculture
School of Life Science, Handong University,
Pohang, Korea diets. These include advanced processing and mixture of feed with other feed compo-
nents to balance antinutritional factors. The impact of dietary soybean oil on gut mi-
Correspondence
Zhigang Zhou, Key Laboratory for Feed crobiota has also been investigated but to a lesser extent than SBM. As the
Biotechnology of the Ministry of Agriculture, gastrointestinal tract has been suggested as one of the major routes of infection in
Feed Research Institute, Chinese Academy of
Agricultural Sciences, Beijing, China. finfish species and crustaceans, the effect of soybean products on the gut microbiota
Email: zhouzhigang03@caas.cn is important to investigate. Several studies have focus on supplementation of SBM on
and
Einar Ringø, College of Fishery Science, the adverse responses of the innate immune system as immunological mechanisms are
Faculty of Biosciences, Fisheries and likely involved in the underlying pathology. However, the precise cause of the inflam-
Economics, UiT The Arctic University of
Norway, Tromsø, Norway. matory process has not yet been clarified, even though some investigations have sug-
Email: Einar.Ringo@uit.no gested that alcohol-­soluble antinutritional factors, especially soy saponins, are
Funding information potential causative factors. Possible interactions between soybean products and in-
National Research Foundation of nate immune system in several finfish species and crustaceans are discussed.
Korea, Grant/Award Number: NRF-
2014R1A2A1A11051899 and NRF-
2015R1D1A1A01056959 KEYWORDS
aquatic animals, diseases, fish health, gut bacteria, Physiology, Salmonids, Tilapia

1 | INTRODUCTION aquafeeds requiring higher protein and lower carbohydrate levels

On a global scale, fisheries’ landings have remained constant at about
90 million tons per annum for the past decades, whereas aquaculture
output has been increasing ca. 80 g kg−1 per annum and now supplies
about 78 million tons (http://www.fao.org/publications/sofia/2016/
en/) (FAO 2016). To sustain increasing rates of aquaculture produc-
tion, it is essential to have a matching increase in the volume of fish
feeds. The requirement for aquafeed has been estimated to reach 60
million tons by 2020. Although this is only a small portion of the global
animal feed production (ca. 620 million tons), the specific nature of
compared to other animal feeds. Normally, the raw materials for these
ingredients were fish meal (FM) and fish oil (FO). However, the global
annual production of FM and FO is only 6 and 1 million tons, respec-
tively, with the main sources being designated pelagic fisheries, mainly
from the Atlantic, Chile and Peru. FM and FO are also produced from
trimmings, offal and/or by-­catch, although to a limited extent (FAO,
2009, FAO, 2016; Olsen, Waagbø, Ringø, & Lall, 2010).
The figures on oil and meal production have remained fairly sta-
ble for the last 20 years, and there are no prospects for increase.
Consequently, since the 1990s, there have been increased efforts by

644  |  wileyonlinelibrary.com/journal/anu

© 2017 John Wiley & Sons Ltd Aquaculture Nutrition. 2018;24:644–665.
ZHOU et  al |
      645

feed manufacturers to find alternative sustainable feed sources to be

Protein isolates
used in aquaculture diets. Among the first sources to be explored were
various soybean products (Francis, Makkara, & Becker, 2001). It was a
reasonable choice in many ways since soybeans have been the most

950
860
important oilseed crop. With an estimated harvest of 315 mill metric

40

45
7

1
tons in 2014/2015, soybeans contribute to 61% of the total worlds
total oilseed supply (US Department of Agriculture; USDA Foreign
Agricultural Service, statista).

Protein concentrates
Worldwide, soybean proteins represent a major source of amino
acids for human and animal nutrition (for review see the book ed. by
El-­Shemy, 2011). However, soybean products proved to be more of
a challenge for aquaculture species than originally anticipated. First,
despite a relatively high crude protein (CP) content (ca. 480 g/kg dry

950
650

200

40
50
7
matter in standard meals), the level was a limiting factor; normally, FM
contains 500–700 g protein per kilo. This limited their inclusion lev-
els in intensive aquaculture diets (Drew, Borgeson, & Thiessen, 2007).
Furthermore, the relatively high content of carbohydrates is a chal-

Dehulled solvent
lenge for many carnivorous fish which do not respond well to high
levels. Some of these challenges can be lowered using processed soy-

extracted
bean products with lowered carbohydrate and higher protein levels

880
480

300
as in protein concentrates (650 g kg−1 CP) and isolates (860 g kg−1

10

30
60
CP), respectively (Table 1). Compared to some other vegetable prod-
ucts, soybean meals (SBMs) have favourable amino acid profile. It is a
good source for lysine, but limiting for most fish species with being low
in methionine (Lim, Webster, & Lee, 2008). To prevent reductions in

Soybean hulls
growth rate at high inclusion levels of soybean protein, balancing with
other protein or crystalline amino acids are required (Burr, Wolters,
910
120

317

401
21

51
Barrows, & Hardy, 2012; Gaylord & Barrows, 2009).
The most serious challenges using soybean products are, however,
their content of antinutritional factors. These are either natural com-
Toasted full fat meal

pounds found in soybeans or their metabolites transformed in living

systems that will negatively affect fish performance. Broadly speak-
ing, they can affect utilization of proteins (e.g., protease inhibitors,
tannins), minerals (e.g., phytates) or vitamins (antivitamins). Other are
880
460
180
250

50
66
often referred to as miscellaneous substances having various effects
like lectins (hemagglutinins), saponins and phytoestrogens (Drew
T A B L E   1   Composition of soybean products during processing

et al., 2007; Francis et al., 2001).

Full fat soybeans

2 |  ANTINUTRITIONAL FAC TORS AND

FEED PROCESSING
900
380
180
100

160

Data from FAO (2002) and Feedstuffs (2016)

40

Raw soybeans are inedible to all monogastric animals and need to be

processed to reduce the level of antinutrients (ANFs) prior to use in
feeds. As some of the most damaging ANFs (e.g., trypsin inhibitors
Proximate composition g/kg

(Kunittz & Bowman-­Birk), hemagglutinins (lectins) and antivitamins)

Carbohydrates (soluble, by

are heat labile, the traditional way to reduce their content has been
through heat inactivation. The process includes short-­term exposure
to high temperatures (e.g., roasting, boiling or extruding) as shown in
Crude protein
Ether extract

Table 2. Different heating processes can reduce the ANF content, but
difference)
Crude fibre
Dry matter

they are not completely eliminated. They will thus follow the product
through the production line. It is also important to note that many
Ash

ANFs like tannins, phytoestrogens and some phenolic compounds,

 |
646       ZHOU et  al

T A B L E   2   Effect of thermal processing

Raw soybeans Extrusion Cooked Toasted Roasted
on antinutritional factors in soybean. After
Trypsin inhibitor 0.0154 0.0061 0.0023 0.0073 0.0071 Ari, Ayanwwale, Adama, and Olatunji
(g/kg) (2012)
Phytic acid 3.45 1.02 1.13 1.78 0.97
(g/100 g)
Protein solubility 850 760 830 770 640
index (g/kg)

Extrusion, cooking (1:1 water: beans, 100°C for 30 min), toasting (pan, 100°C for 30 min) and roasted
(dry heating, 100°C for 30 min).

saponins, glucosinolates, oligosaccharides, antigenic proteins (e.g.,
glycinin and ß-­conglycinin) and phytates are heat stable, and will not
be significantly affected by the heat treatment.
Many carnivorous fish species have proven to be more sensitive to
remnants of the heat labile ANFs than terrestrial animals. Furthermore,
many of the heat stable ANFs have also caused problems (Drew et al.,
2007; Francis et al., 2001; Krogdahl, Penn, Thorsen, Refstie, & Bakke,
2010). To improve their suitability in fish, major efforts have been in-
vested into producing soybean products with higher protein levels and
lower levels of both heat labile and heat stable ANFs. A brief outline of
some main processes is given in Figure 1 and the changes in chemical
content in Table 1. The full fat meal produced from heating of raw
beans will produce a product with similar chemical content but with
reduced levels of ANFs. To reduce the fibre content, the soybeans can
be cleaned and cracked open by passing them over roller mills. This is
followed by dehulling, the removal of the hulls producing a full fat meal
that is lower in fibre, but with a higher content in crude protein and
carbohydrates. This product can be used in aquaculture, but would
need heating as for whole soybeans to reduce heat labile ANF.
Dehulled soybeans are also the starting point for further pro-
cessing of the soy. One typical pathway is to produce flakes followed
by lipid extraction to produce a lipid phase and defatted SBM. Lipid

Toasting Soybean

Full fat soy

Cleaning
Cracking
Hulls Dehulling
Conditioning
Flaking

Lecithin
Lipid Full fat flakes
Refined extraction
soybean oil

Defatted soy flakes Toasting

Alcohol Aqueous extraction Grinding Dehulled

extraction Separation extrusion soybean meal
Precipitation
pH adjustment
Hulls

Soy protein Soy protein isolate Textured soy Soybean

concentrate

Extrusion Enzyme hydrolysis

heating

Texturized Low antigen

SPC isolate
F I G U R E   1   Outlines of various soybean
processing methods. Modified after Herzog
Low antigen
concentrate Möller and USSEC U.S. Soybean Export
Council
ZHOU et  al |
      647

removal is often intended to lower the content of linoleic acid (18:2

Chen, Wang, Song, and Ma

Anderson and Wolf (1995)

Anderson and Wolf (1995)
Anderson and Wolf (1995)

Hei, Li, Ma, and He (2012)

n-­6) in the fish diets. The meal fraction is then heated to remove re-

Jankowski et al. (2009)

Extruded SPC and low-­antigen SPC have significantly lower ANF levels than soybeans, soybean meal and soy flour and are the preferred products for use in aquafeeds for species sensitive to soy ANF’s.
maining hexane and to reduce ANF. This produces a dehulled defatted
SBM. The hulls can be returned to the meal producing hulled defatted
SBM.

References
These processes, however, have very little effect on the heat

(2014)
stable ANF like non-­starch polysaccharides, saponins, phytates, phy-
toestrogens and protein antigens (Table 3, Francis et al., 2001; Drew
et al., 2007). These can be reduced by alcohol (methanol/ethanol) or
aqueous extractions of the meals giving soybean concentrate and
soybean isolate, respectively. Alcohol extraction removes some sol-

Protein isolate
uble carbohydrates increasing the CP content to around 700 g kg−1.
The majority of fibres are, however, not soluble and will remain in the

1.4–29
meal. Extraction also lowers levels of trypsin inhibitors, glycinin, ß-­

<0.2
9–2

13

4
8
conglycinin, saponins, and oligosaccharides, and extrusion and heat
treatment will further lower the content of remaining heat labile ANFs
giving more specialized products like low-­antigen soybean concen-
trates. Solubilizing the protein in water followed by protein precipi-

Protein concentrate
tation removes lipid and carbohydrates from the product (Table 3,
FAO 2002; NRC 2012) increasing the CP to around 900 g kg−1. Some
alcohol-­soluble ANFs like saponins are, however, not well reduced

5.4–7.3
12–21
and can still cause problems for fish (Drew et al., 2007; NRC. National

4.8

25
21
Research Council, 2012).

0
To improve soybean utilization in fish, researchers and producers
have explored new processing pathways like bioprocessing, fermenta-
tion, or inclusions of enzymes like phytase to reduce phytin content Toasted flour

(increasing mineral uptake). Enzymatic hydrolysis has the potential to

reduce the level of many ANFs and enhance nutrient utilization. For 7.9–9.4
13–18

example, enzyme-­treated SBM has reduced levels of ANF like glycinin

50
6
and β-­conglycinin. Further, treatment with phytase will reduce phy-
tin content and enhance phosphorous availability (Table 4, Goebel &
T A B L E   3   Comparison of the antinutritional factor levels in various soy products

Stein, 2011). Fermentation using the bacteria Aspergillus oryzae, for

example, eliminates protease inhibitors (Hong, Lee, & Kim, 2004),
Toasted meal

oligosaccharides, and many other meal antigens (Cervantes-­Pahm &

Stein, 2010). However, such alternative treatment methods will add
15–18

144

118

to the cost of products which could make them unavailable to most

50
5

aquaculture facilities. Rather, it is therefore a tendency in commercial

aquaculture to mix several vegetable products to improve the nutri-
ent amino acid profiles, and to reduce the impact of individual antinu-
Raw soybeans

tritional factors. Regardless, soybean products are still a dominating

vegetable ingredient in aquaculture. In Norway, for example (mainly
100–23
16–27

for salmon aquaculture), soybean concentrate was the largest single

50
124

104
5

meal inclusion (213 g kg−1) closely followed by FM (195 g kg−1) in 2012

(Ytrestøyl, Aas, & Åsgård, 2015), while other vegetable meals were in-
cluded at levels of 60g/kg diet or less. These processes will not only
Trypsin inhibitor activity (g/kg)

cause major changes in the composition of the products, but they are
ß-­conglycinin antigen ppm

also likely to modulate the gut microbiota as nutrient substrates are

Oligosaccharides (g/kg)
Glycinin antigen ppm

changing. Direct comparison of the various products in fish is there-

Phytic acid (g/kg)

fore challenging.
Saponins (g/kg)

The gut microbiota of fish constitutes a great number of cells, and

these cells and their metabolites play important roles in host diges-
tive function, gastric development, mucosal tolerance, immunity and
disease resistance (Bansal, Alaniz, Wood, & Jayaraman, 2010; Corr
 |
648       ZHOU
Defatted soybean
Proximate composition (g/kg) meal HP-­200
Trypsin inhibitor TI/mg 5.7 3.1
Glycinin antigen ppm 420 17
β-­conglycinin antigen ppm 130 0.003
Neutral detergent fibre 76 118
Acid detergent fibre 45.16 54
HP-­200, processed at fast rate; HP-­310, processed slower than HP-­200; HP-­340, processed with
phytase added.
et al., 2007; Holtug, Rasmussen, & Mortensen, 1988; Li, Wang, Xu,
Magarvey, & McCormick, 2011; Shimada et al., 2013; Smith et al.,
2013; Vinolo, Rodrigues, Nachbar, & Curi, 2011). In fact, in the ab-
sence of gut microbiota, the digestive tract fails to differentiate fully,
lacks brush border intestinal alkaline phosphatase activity, presents
immature patterns of glycan expression, displays reduced epithe-
lial proliferation and a reduction in goblet and enteroendocrine cells
(Bates et al., 2006; Rawls, Samuel, & Gordon, 2004).
Immunological effects of SBM or SBO have been less examined in
comparison with studies evaluating its effect on growth performance
and gut histology. In recent years, however, the effect of dietary SBM
or SBO on the immune systems of finfish and crustaceans are being
pursued.
The present review addresses the effect of dietary soybean prod-
ucts on gut microbiota and immunological parameters of aquatic an-
imals. To give the readers satisfactory information on the effects of
dietary soybean products, the authors include some information from
endothermic animals when needed. The information presented on
finfish is organized according to the current recognized taxonomical
structure (FishBase 2015).
3 |  EFFECTS OF SOYBEAN PRODUCTS ON
GUT MICROBIOTA
As in endothermic animals, the intestinal bacterial community of fish
assist the function of digestion, growth, reproduction and improve
health (Ganguly & Prasad, 2012; Ghanbari, Kneifel, & Doming, 2015;
Llewellyn, Boutin, Hoseinifar, & Derome, 2014; Merrifield & Rodiles,
2015; Montalban-­Arques et al., 2015; Ray, Ghosh, & Ringø, 2012). In
addition, some intestinal bacteria can also destroy toxins that can be
harmful or fatal to its host (e.g., Duar et al., 2014; Harishankar, Sasikala,
& Ramya, 2013; Rowland, 1988; Singh & Walker, 2006; Young, Zhou,
Yu, Zhu, & Gong, 2007). Great efforts have also been made to find
dietary supplements that ensure that benign or beneficial microbes
dominate the intestinal microbiota of fish (Dimitroglou et al., 2011;
Merrifield et al., 2010; Ringø, Olsen et al., 2010; Ringø et al., 2016).
The gut microbiota of endothermic animals as the case with fish is
classified as autochthonous or indigenous, when they are able to adhere
and colonize the host’s mucus layer or gut epithelial surface, or alloch-
thonous, when they are incidental visitors in the GI tract, and are ex-
pelled after some time without colonizing (Kim, Brunt, & Austin, 2007;
et  al
T A B L E   4   Effect of bioprocessing on the
content of some antinutritional factors in
HP-­310 HP-­340
soybean products after Goebel and Stein
2.4 1.8 (2011)
0.33 0.09
0.004 0.005
126 99
53 52
Ringø & Birkbeck, 1999; Ringø, Olsen, Mayhew, & Myklebust, 2003).
The adherent bacteria may play an important role in health and disease
control of fish, and in this regard, it is of importance to bear in mind
that the GI tract of fish is one of the major infection routes for some
pathogens (Birkbeck & Ringø, 2005; Bøgwald & Dalmo, 2014; Groff &
LaPatra, 2000; Harikrishnan & Balasundaram, 2005; Ringø, Myklebust,
Mayhew, & Olsen, 2007; Ringø et al., 2003; Ringø, Løvmo et al., 2010).
Compared to the numerous studies describing the dietary effect
on fish gut microbiota (Ringø et al., 2016), less information is available
about the effects of soybean products on intestinal bacterial commu-
nity of finfish and crustaceans (Table 5).
Even though the traditional culture-­based technique possesses
rather low sensitivity for measuring composition, structure and stabil-
ity of bacteria colonizing fish GI tract, the technique is able to reveal
differences due to minor dietary alterations, for example adherent
bacteria in PI and distal fermentation chamber of Atlantic cod (Gadus
morhua L.) fed different SBM products (Figure 2).
3.1 | The Effect of SBM on Gut Microbiota
While much effort has focused on evaluating the extent of SBM-­
induced histological damage, SBM-­induced enteritis (SBMIE) (e.g.,
Bakke-­McKellep, Press, Baeverfjord, Krogdahl, & Landsverk, 2000;
Bakke-­McKellep, Froystad et al., 2007; Bakke-­McKellep, Penn et al.,
2007; Bakke-­McKellep, Koppang et al., 2007; Hedrera et al., 2013;
Krogdahl, Bakke-­Mckellep, Roed, & Baeverfjord, 2000; Metochis et al.,
2016; Rumsey, Siwicki, Anderson, & Bowser, 1994), the effects on the
intestinal microbiota of fish were not reported until 2006. However,
as the importance of the gut microbiota and our awareness of this
complex microbial ecosystem have increased the interest in the fac-
tors that might modulate the intestinal microbial communities (Ringø
et al., 2016). Consequently, there are an increased number of stud-
ies addressing the impact of dietary SBM on fish intestinal microbiota
(Table 5). One major driving force for these studies is the possible
modulation of the intestinal microbiota by SBM towards an undesira-
ble community that can induce mucosal inflammation (Tamboli, Neut,
Desreumaux, & Colombel, 2004; Turroni et al., 2014).
Some publications addressing the effect of SBM on gut microbi-
ota were discussed in the review of Merrifield, Olsen, Myklebust, and
Ringø (2011), and to avoid duplication, these studies reviewed in the
aforementioned review are not discussed in this subsection; only re-
sults are presented in Table 5.
ZHOU et  al       649|
T A B L E   5   Studies investigated the effect of soybean meal (SBM), soy protein concentrate (SPC) and soybean oil (SO) on gut microbiota

Fish species/weight Soybean product Length of adm. Results by feeding SBM/SPC/SO References

Rainbow trout
21.1 ± 1.4 g SBM (450 g/kg) 8 weeks ↓ culturable bacteria, Lactobacillus spp., Sphingomonas Heikkinen et al. (2006)a
spp.
↑ Bacillus spp., Chryseomonas spp.

~40 g SBM (450 g/kg) 16 weeks → total culturable aerobic levels, Micrococcus spp. Merrifield, Bradley,
↓ Aeromonas spp., Vibrio spp. Baker, Dimitroglou, and
↑Actinomycetales, Psychrobacter spp., Saccharomyces Davies (2009)a
spp.
1.56 ± 0.9 kg SBM (300 g/kg) 8 weeks ↑no. of clones identified as Carnobacterium Mansfield et al. (2010)
maltaromaticum
↓ no. of different sequences in library

~510 g SBM (300 g/kg) 8 weeks ↑ Firmicutes: Proteobacteria ratio Desai et al. (2012)
DGGE analysis revealed low similarity indices
between SBM-­fed fish and the control
Atlantic salmon
172 g SBM (250 g/kg) 3 weeks ↑autochthonous bacteria in MI and DI, allochthonous Bakke-­McKellep, Penn
in DI et al. (2007)a
→ no. of genera and strains
↑ Brevibacterium, Enterococcus, yeast
↓Marinilactobacillus psychrotolerans,
C. maltaromaticum
242 ± 8 g SBM (436 g/kg) 4 weeks → viable counts Ringø, Sigmund
↓ Carnobacterium spp., Bacillus spp. Sperstad, Kraugerud,
and Krogdahl (2008)a
1204 ± 34 g SPC (50 g/kg) ↑bacterial diversity, Escherichia coli, a Green et al. (2013)
Pseudomonadales
144.5 ± 2.3 g SBM (378 g/kg) 35 days → total and viable counts Navarrete et al. (2013)
↑ Aeromonas Via, Sporosarcina equimarina
305 ± 69 g SPC (200 g/kg) 12 weeks →total autochthonous bacteria (proximal intestine; Hartviksen et al. (2014)
PI), total allochthonous bacteria, allochthonous
community composition and total autochthonous
bacteria (DI)
↑autochthonous Enterobacteriaceae, Bacilli-­like,
Lactobacillaceae, Streptococcaceae in PI
↓ autochthonous Vibrionaceae in PI
↑ autochthonous Bacilli-­like, Streptococcaceae in DI

~133 g SBM (200 g/kg) 80 days ↓the diversity indices in DI, Weissella confusa in the Reveco et al. (2014)
DI, proportion of Photobacterium in MI
↑relative abundance of Firmicutes compared with
the FM group, abundance of Lactococcus lactis
subsp. Lactis in MI
→ Photobacterium in DI

~5 g SBM (100 g/kg) 6 weeks ↑total microbial numbers in digesta, J.L.G. Vecino &
Peptostreptococcus, Kluyvera and other closely S. Wadsworth
related representatives of Enterobacteriaceae ­(unpublished data)b
↓ Sphingomonas
Atlantic cod
  ~534 g SBM (246 g/kg) 84 days ↑ allochthonous bacterial level in FG, HG Refstie et al. (2006)a
→ allochthonous bacterial level in HC
↓ autochthonous bacterial level in FG, HG and HC
  ~534 g SBM (246 g/kg) 84 days Modulated gut microbiota. ↑Chryseobacterium and Ringø, Sperstad,
Psychrobacter Myklebust, Refstie, and
Krogdahl (2006)a

(Continues)
 |
650       ZHOU et  al

T A B L E   5   (Continued)

Fish species/weight Soybean product Length of adm. Results by feeding SBM/SPC/SO References

  ~534 g BPSBM (214 g/kg) 84 days →population levels of adherent and allochthonous Ringø et al. (2006)a
bacteria in FG, HG and HC
Modulated gut microbiota.
↑Psychrobacter
Gilthead seabream
~24 g SBM (313 g/kg) 9 weeks ↑ species richness, Shannon-­Weaver index Dimitroglou et al.
(2010)a
Grass carp
 Ctenopharyngodon SBM (13 g/kg) 8 weeks ↑Pseudomonas putida Aeromonas sp.DH69 Huang (2008)b
idella (weight not Actinobacterium Bacilli bacterium
given)
Allogynogenetic silver crucian carp
 Carassius auratus♀ SBM (300 g/kg) 8 weeks →total culturable aerobic and anaerobic bacteria, Cai et al. (2012)a
x Cyprinus carpio♂ presumptive E. coli, Aeromonas, Bifidobacterium,
(24.7 g ± 0.4 g) Clostridium perfringens
Goldfish
 Carassius auratus SBM (355 g/kg) 8 weeks → on gut microbiota determined by DGGE Raggi and Gatlin (2012)
(15 g)
Three cyprinid SBM (40 g/kg) 8 weeks Modulation of the allochthonous gut microbiota. Li et al. (2015)
species ↓Proteobacterium clone (EF707282.1), Cetobacterium
somerae (AB353124), Bacillus subtilis, Anoxybacillus
flavithermus
Hybrid tilapia
 Oreochromis SBM 8 weeks ↑Plesiomonas sp. BTOK4 Aeromonas aquariorum Zhang, Xu et al. (2014)
niloticus ♀ x
Oreochromis
aureus ♂ (~2 g)
Arctic charr

 ~250 g SBO (208 g/kg) Not given →total culturable aerobic bacteria Acinetobacter spp. Ringø et al. (2002)a
and Carnobacterium spp. were only present in SBO
fed fish, while Micrococcus spp. were only present in
the FO fed charr
Channel catfish
 Ictalurus punctatus SBO (80 g/kg) 120 days → culturable lactic acid bacteria counts Santerre et al. (2015)
(6.83 ± 0.2 g)
Pacific white shrimp
 Litopenaeus SBO 8 weeks ↑Enterobacteriaceae, Aeromonadaceae Zhang, Sun et al. (2014)
vannamei ↓Rhizobiaceae Bacteroidaceae was only present in
the SBO group

↑, increase; →, no change; ↓, decrease.

FG, foregut; HG, midgut; HC, hindgut chamber.
a
Studies discussed in the review of Merrifield et al. (2011).
b
Studies discussed in the review of Ringø et al. (2016).

frequently observed sequences were identical to Carnobacterium (pis-

3.1.1 | Salmonidae
3.1.1.1 | Rainbow trout (Oncorhynchus mykiss Walbaum)
Mansfield et al. (2010) evaluated the effect of FM and SBM (Federation
Cooperatives Limited, Saskatoon, SK, Canada) (300 g/kg) on the al-
lochthonous DI microbiota of triploid female rainbow trout (~1.6 kg)
by three cpn60 universal clone libraries, resulting in 1,000 and 1,181
sequences from FM and SBM, respectively. When all the sequences
were combined, 32 different sequences were noticed. The most
cicola) maltaromaticum and accounted for 55 and 97.2% of the clones
from the FM and SBM group, respectively. Overall, highest diversity
was noticed from fish fed FM (14 different sequences) and only four
different sequences in the SBM library.
In a later study with rainbow trout, Desai et al. (2012) investigated
the influence of SBM (Federation Cooperatives Limited, Saskatoon, SK,
Canada) and FM on the commensal intestinal microbiota by pyrose-
quencing of cpn60 PCR products and 16S rRNA DGGE. Pyrosequencing
ZHOU et  al
F I G U R E   2   Indigenous adherent
bacteria isolated from the gut wall of (a)
the proximal intestine and (b) the distal
fermentation chamber of Atlantic cod
(Gadus morhua L.) fed; fish meal (FM),
soybean meal (SBM) or bioprocessed
soybean meal (BPSBM) after Refstie et al.
(2006)
revealed that SBM inclusion (300 g/kg) was associated with higher
Firmicutes: Proteobacteria ratio than control fed fish (FM). Differences
between the microbial community of SBM-­fed fish and the control
were also observed in DGGE profiles, as the similarity indices between
SBM-­fed fish and the control was 470 g kg−1. Whether the changes in
microbial communities may have been caused by changes in intesti-
nal mucosal morphology and immune responses were not investigated
and to conclude additional investigations have to be carried out.
3.1.1.2 | Atlantic salmon (Salmo salar L.)
Green, Smullen, and Barnes (2013) investigated the influence of FM
and soybean protein concentrate (SPC; 50 g/kg) on intestinal micro-
biota of Atlantic salmon by terminal restriction fragment length poly-
morphism (T-­RFLP) and 16S rRNA clone library analysis. The SPC diet
resulted in modulation of the intestinal microbiome by increasing the
bacterial diversity and increased Escherichia coli which was absent in
salmon fed FM. In addition, a pseudomonadales was more frequently
revealed in fish fed SPC.
In a 35 days feeding trial with Atlantic salmon, Navarrete et al.
(2013) evaluated the effect of SBM HI Pro (378 g/kg) supplementation
and FM (510 g/kg) on allochthonous microbiota community in DI. Total
and viable counts were not significantly (p > .05) affected by dietary
manipulation, but bacterial composition evaluated by principal com-
ponent analysis (PCA) was grouped according to the diet, except for
day zero. PCA analysis revealed that Aeromonas VIb and Sporosarcina
aquimarina were correlated with the SBM diet, while Microbacterium,
Pseudomonas, Lactococcus lactis sp. cremoris and Aeromonas VIa were
correlated with the FM diet.
Hartviksen et al. (2014) revealed no dietary effect of soy protein
concentrate (SPC) on total autochthonous bacteria isolated from PI
and total allochthonous and total autochthonous bacteria isolated
from DI of Atlantic salmon by qPCR analysis. However, significant
|
      651
(p = .05) effect was observed with regard to community composition.
An increase was noticed in autochthonous Enterobacteriaceae, Bacilli-­
like, Lactobacillaceae and Streptococcaceae in PI, and Bacilli-­like
and Streptococcaceae in DI by SPC feeding. In contrast, a significant
(p = .05) decrease was revealed in Vibrionaceae in PI.
Reveco, Øverland, Romarheim, and Mydland (2014) investigated
the intestinal microbiota in MI and DI of Atlantic salmon fed FM
and SBM (Deno-­Soy F, solvent-­extracted and solvent-­toasted SBM,
Denofa, Fredrikstad, Norway) (200 g/kg) by DGGE analysis. The diver-
sity indices were reduced in DI by SBM feeding, and the SBM diet gave
rise to a higher relative abundance of Firmicutes compared with the
FM group. Furthermore, the abundance of Lactococcus lactis subsp.
lactis increased in the MI, while a reduction in Weissella confusa was
reported in the DI of fish fed the SBM diet. The proportion of bacteria
belonging to genus Photobacterium was higher in MI of the FM group,
but in DI, the proportion of Photobacterium was not affected by dietary
manipulation. The authors suggested that the shift in the intestinal
bacterial community could be involved in SBMIE, however, to fully
conclude additional investigations have to be carried out.
In contrast to the literature available on the effects of SBM on the
gut microbiota of salmonids, less is known about other fish species.
This is partly due to the fact that non-­salmonids are less suscepti-
ble to SBMIE and histological damage. However, some papers have
addressed the effect of SBM on gut microbiota of non-­salmonids
(Table 5).
3.1.2 | Cyprinidae
Huang (2008) compared the effect of dietary inclusion of SBM (13 g/
kg) and casein meal (CM; 10 g/kg) on the autochthonous intestinal
microbiota of grass carp (Ctenopharyngodon idella). After 8 weeks
feeding, the microbiota from the whole intestine was analysed by
 |
652       ZHOU
16S rRNA PCR-­DGGE. Clear differences were revealed between the
microbiota of the SBM group and the CM group showing only 26%
similarity (p < .05); determined by the un-­weighted pair group method
using the arithmetic mean algorithm (UPGMA). Bacteria isolated from
the CM group were identified; uncultured Lachnospiraceae bacterium,
uncultured Lactobacillus, uncultured Clostridium spp. and uncultured
Proteobacterium, while bacteria isolated from the SBM group were
identified as Pseudomonas sp., Aeromonas sp., uncultured bacteria, un-
cultured Actinobacterium and uncultured Bacillus spp.
Raggi and Gatlin (2012) evaluated four probiotics diets based on
FM and SBM on gut microbiota of goldfish (Carassius auratus) and
revealed no difference in microbiota by denaturing gradient gel elec-
trophoresis. The main reason for this observation may be due to the
−1
dietary incorporation of chromic oxide at 10 g kg may have reduced
the quantity and complexity of the bacterial community as reported by
Ringø (1993) for Arctic charr (Salvelinus alpinus L.).
In a recent study, the effect of partial or complete replacement
of SBM (40 g/kg) by intestinal casing meal [ICM; prepared from the
waste water of enteric coating and heparin processing (Shi, 2002)]
or a mixture of ICM and monosodium glutamate (YMG) was used to
evaluate the effect on the allochthonous gut microbiota of three cage-­
cultured cyprinid species (Li et al., 2015). The allochthonous bacterial
diversity was modulated by feeding ICM and YMG as some bacterial
species were significantly stimulated; Bacillus subtilis in black carp
(Mylopharyngodon piceus) and blunt snout bream (Megalobrama am-
blycephala), Anoxybacillus flavithermus in black carp (Mylopharyngodon
piceus) and Proteobacterium and Cetobacterium somerae in blunt snout
bream (Megalobrama amblycephala).
3.1.3 | Cichlidae
3.1.3.1 | Hybrid tilapia (Oreochromis niloticus ♀ X Oreochromis
aureus ♂)
Zhang, Xu et al. (2014) investigated the effects of replacing dietary
SBM or cottonseed meal (CSM) by completely hydrolysed feather
meal (defatted rice bran as the carrier; CHFM) on the composition
of adherent gut bacteria of hybrid tilapia. After 8 weeks of feeding,
the microbiota from the whole intestine was analysed by 16S rRNA
PCR-­DGGE. The results showed that CHFM induced modulation of
the intestinal microbiota in hybrid tilapia and prevented colonization
of potentially harmful species in the intestinal tract. Plesiomonas sp.
BTOK4 and Aeromonas aquariorum were decreased in the CHFM12/
CSM (120 g kg−1 CSM was replaced with CHFM) group.
The reason for the differing outcomes in the culturable bacterial
communities is somewhat unclear, but it may be related to: (i) different
feeding duration, (ii) different SBM inclusion levels, (iii) different SBM
characteristics and different producers, (iv) different culture conditions
and/or (v) other differences in the experimental rearing trial.
Many of the previous studies addressing the effects of dietary SBM
on the gut microbiota of finfish were based on cultivation. However, as
the use of media to cultivate microbes for the determination of micro-
bial abundance and identification do not represent a correct picture
of the intestinal bacterial community, culture-­independent techniques
et  al
as described by Zhou et al. (2014), Ghanbari et al. (2015) and Ringø
et al. (2016) need to be included in future studies. According to Zhou
et al. (2014), the cultivability of communities in the intestine of many
fish species can be as low as <0.1%. Furthermore, investigations need
to be extended to other aquatic species than salmonids as SBM is one
of the commonly used plant proteins incorporated into aquafeeds
(Bakke-­McKellep & Refstie, 2008; Barrows et al., 2008; Bendiksen,
Johnsen, Olsen, & Jobling, 2011; Gatlin et al., 2007; Hansen & Hemre,
2013; Hemre et al., 2009; Médale et al., 2013). In addition, future
studies should focus on the autochthonous bacteria as they are in in-
timate contact with the host epithelium stimulating host inflammatory
responses and/or improving fish health and ability of gut microbiota to
produce short chain fatty acids (SCFAs) (e.g., Hoseinifar, Mirvaghefi,
Amoozegar, Merrifield, & Ringø, 2017; Kihara & Sakata, 2002). For
example, butyrate is the main energy source for colonic epithelial
cells and thus associated with maintenance of the epithelium and has
the potential to stimulate the immune system and resistance against
pathogens (Maslowski & Mackay, 2010). Moreover, it has been pro-
posed that SCFAs modulates lipid synthesis (Marcil et al., 2002).
3.2 | The Effect of Soybean Oil (SBO) on
Gut Microbiota
To our knowledge, four studies have assessed the effect of dietary
SBO on autochthonous gut microbiota of aquatic animals (Lødemel
et al., 2001; Ringø et al. 2001; Ringø et al., 2002; Zhang et al. 2014b;
Santerre et al., 2015.
3.2.1 | Salmonidae
3.2.1.1 | Arctic charr (Salvelinus alpinus L.)
Lødemel et al. (2001) revealed autochthonous bacteria closely asso-
ciated with microvilli in the midgut region of charr fed SBO prior to
challenge with A. salmonicida ssp. Salmonicida (Figure 3). When Arctic
charr were challenged with A. salmonicida, only a few bacteria were
associated with microvilli of the midgut of infected fish. Furthermore,
light microscopy studies of the midgut epithelium of the Arctic charr
fed SBO prior to challenge revealed few goblet cells, while infected
fish with external signs of furunculosis had greater abundance of
goblet cells. The greater prevalence of goblet cells, which increased
mucus production, supports the suggestion that sloughing off mucus
is a protective response against bacterial infections.
Ringø et al. (2002) addressed the effects of SBO and FO on the
aerobic gut bacteria of Arctic charr before and after challenge with
A. salmonicida. This study was discussed in the review of Merrifield
et al. (2011), and readers with special interest in this study are referred
to the above-­mentioned review.
3.2.2 | Siluriformes
3.2.2.1 | Channel catfish (Ictalurus punctatus)
Santerre et al. (2015) revealed no effect on culturable lactic acid bac-
teria (LAB) counts when channel catfish was fed diets differing in oil
ZHOU et  al
F I G U R E   3   Transmission electron microscopy micrograph of the
midgut of Arctic charr (Salvelinus alpinus L.) fed a diet-­containing SBO.
Note the substantial numbers of bacteria (arrows) associated with
the microvilli (MV) of the enterocytes. X 3.750 magnification after
Lødemel et al. (2001)
source (FO or SBO) and supplementation of commercial probiotic, de-
rived from 14 different microorganisms. However, LAB was not iden-
tified by 16S rRNA gene sequencing. Phenotypic males were used in
this study, and this open for the speculation that differences in LAB
composition may occur between gender, as some studies on aquatic
animals have revealed differences in gut microbiota between male and
female (Iehata, Valenzuela, & Riquelme, 2015; Li et al., 2016).
3.2.3 | Penaeidae
3.2.3.1 | PACIFIC white shrimp (Litopenaeus vannamei)
There is evidence, albeit limited, showing that healthy and diseased
shrimp have distinct gut bacterial communities (Cheung et al., 2015;
Xiong, Dai, & Li, 2016; Xiong et al., 2015; Zheng et al., 2016). The
Pacific white shrimp is a very important culture species, but little in-
formation is available on the effect of feed nutrients on the intestinal
microbiota. Zhang, Sun et al. (2014) examined the intestinal bacte-
rial composition of Pacific white shrimp fed six diets with different
lipid sources using the Illumina-­based high-­throughput sequencing
method. The results revealed that Bacteroidaceae was only present
in SBO; however, the prevalence rate was low (0.01%–0.08%). The
prevalence of Rhizobiaceae decreased significantly by SBO feeding,
while the prevalence of Aeromonadaceae and Enterobacteriaceae in-
creased in SBO group.
4 | IMMUNOLOGY
Many studies attempt to uncover ways to balance out the adverse ef-
fects that might be caused by SBM or SBO supplemented in diets. The
immunological studies predominantly concentrate on innate immune
parameters modulated by the inclusion of SBM or SBO (Table 6). As
|
      653
the innate immune system directly influences the adaptive immune
system, current studies need to be further expanded to see if and how
dietary SBM or SBO may alter adaptive immune responses as well.
In addition, future studies should focus on the immunological param-
eters, especially innate immune parameters that can directly represent
the health status of finfish and crustaceans. Immune responses and
disease resistance from a general nutritional context are not reviewed
in this review, and readers with special interest on these topics are re-
ferred to the comprehensive reviews of Kiron (2012) and Oliva-­Teles
(2012).
4.1 | Salmonidae
4.1.1 | Atlantic Salmon (Salmo salar L.)
It is known that an SBM-­containing diet causes intestinal inflamma-
tion in the DI of salmonid fish; SBMIE (e.g., Baeverfjord & Krogdahl,
1996; Urán et al., 2008; Van den Ingh, Krogdahl, Olli, Hendricks, &
Koninkx, 1991). Krogdahl et al. (2000) examined the effect of the fish
diet containing either solvent-­extracted SBM or alcohol-­extracted
SBM. The fish fed solvent-­extracted SBM showed higher mortality
rate when challenged by A. salmonicida. In addition, the group fed
alcohol-­extracted SBM revealed increased levels of both lysozyme
and IgM in the mid and distal intestinal mucosa. Lilleeng et al. (2009)
studied the early stages of SBM enteropathy in Atlantic salmon by
quantitative PCR analysis. Fish fed SBM showed significantly down-
regulated TGF-­β gene expression on day one of SBM feeding, whereas
reduced expression of interferon-­inducible lysosomal thiol reductase
(GILT) was observed on day three. The authors suggested that down-
regulation of TGF-­β and GILT might lead to the pathogenesis of SBM
enteropathy in Atlantic salmon due to failure to maintain mucosal in-
tegrity in the DI. Sahlmann et al. (2013) investigated transcriptomic
profiling during one-­week feeding of a diet-­containing 200 g kg−1
SBM. Prominent changes in gene expression patterns were observed
on days 3 and 5. Immune-­related genes were upregulated during the
first 5 days: GTPase IMAP family members; NF-­kB-­related genes; and
regulators of T-­cell and B-­cell function. These expression profiles of
immune genes suggest that intestinal inflammation is induced within
a week upon administration of an SBM-­containing diet, which may
in turn negatively influence the growth performance of salmonids.
However, the exact cause and mechanisms behind the inflammation
and other negative effects are not fully understood. Several investiga-
tions indicate that alcohol-­soluble ANFs, especially soy saponins, may
be the causal agent. In a more recent study, Krogdahl et al. (2015)
showed that saponins caused dose-­dependent increases in the sever-
ity of inflammation independent of the basal diet, with concomitant
alterations in digestive functions and immunological marker expres-
sion. In the inflammatory states of SBMIE or SPCIE, plasma immuno-
globulin level (Bakke-­McKellep et al., 2000; Metochis et al., 2016) and
T-­cell numbers (Bakke-­McKellep, Froystad et al., 2007) were signifi-
cantly increased. Although the physiology of the immune modulation
is not completely understood at present, this activated immune re-
sponses may be related to an allergic reaction caused by SBM or SPC.
T A B L E   6   Studies investigated the effect of soybean meal (SBM) and soybean oil (SBO) on immune response
|

Fish species/weight Soybean product Length of adm. Results by feeding SBM/SPC/SBO References
654      

Atlantic salmon
37.0 g for challenge studies 240 g kg−1 solvent-­extracted SBM, 110 g kg−1 3 weeks Solvent-­extracted SBM: ↑ mortality when challenged by A.s. salmoni- Krogdahl et al. (2000)
 620 g for immune alcohol-­extracted SBM, or 180 g kg−1~22 cida challenge
parameter studies g kg−1 SPC Alcohol-­extracted SBM: ↑ lysozyme and IgM
216 g 460 g kg−1 extracted SBM 1, 3, and 7 days ↓ TGF-­β gene expression on day 1 Lilleeng et al. (2009)
↓ GILT gene expression on day 3
500–600 g 200 g/kg (hexane-­extracted (defatted)) SBM 7 days ↑ Immune-­related genes, including GTPase IMAP family members, Sahlmann et al.
NF-­kB-­related genes, regulators of T-­cell and B-­cell function (2013)
Rainbow trout
2.60 ± 0.18 g 100% replacement of protein source 26 weeks ↑ Leucocyte cell numbers Rumsey et al. (1994)
(410 g kg−1) by SBM ↑ Concentrations of plasma protein and immunoglobulin
↑ Neutrophil, monocyte and macrophage activities
6–7 g 60%–70% replacement by SBM 53 days ↓ Innate immune capacity Burrells et al. (1999)
15 ± 2 g 40% replacement of FM with plant protein 60 days → No noticeable negative effects in lysozyme activity and total Jalili et al. (2013)
sources (250 g kg−1 SBM and glutens) antibody concentration
57.8 g Graded cholesterol supplementation on SBM 9 weeks ↑S erum & hepatic superoxide dismutase (SOD), glutathione-­ Deng et al. (2013)
peroxidase, catalase activities
↑ Serum lysozyme activity up to 9 g kg−1 cholesterol
9 g kg−1~12 g kg−1 cholesterol
↑ Survival upon A. hydrophila challenge
Gilthead sea bream
40 g Total substitution by a mixture of 500 g kg−1 6 months ↓ Phagocytic activity Montero et al. (2008)
SBO and 500 g kg−1 LO ↓ Alternative complement pathway activity
36.99 ± 0.20 g 100% replacement by SBO 80 days ↑ TNF-­a and IL-­1β in the intestine Montero et al. (2010)
16.2 ± 0.61 g 20%, 40%, 60% replacement of FM with FBM 84 days ↑ Serum myeloperoxidase level & complement activity Kokou et al. (2012)
−1
16 g 20%, 40%, 60% replacement of FM with SBM 6 months ↑ RBA, TGF-­B1 B2 m in HK in 400 g kg SBM Kokou et al. (2015)
↑ CSF-­1R, signs of inflammation in 60%
Japanese seabass
10.09 ± 0.70 g 33%, 66%, 100% SBO to replace FO 66 days ↓P
 hagocytic index, respiratory burst, lysozyme activity, alternative Xu et al. (2015)
complement pathway
European seabass
20.63 ± 0.12 g MOS inclusion in SBO-­based diets 8 weeks In SBO-­based diets Torrecillas et al.
↓ TCRβ, COX2, IL-­1β, TNF-­α, IL-­8, IL-­6, IL-­10, TGF-­β and Ig (2015)
↑ MHCII
MOS inclusion in SBO-­based diets
↑ IL-­6, TGF-­β and IL-­10
ZHOU

(Continues)
et  al
T A B L E   6   (Continued)
ZHOU

Fish species/weight Soybean product Length of adm. Results by feeding SBM/SPC/SBO References
et  al

European seabass
283 g 1 or 2 g/kg soya saponins 59 days No effects on expressions of AIP, Malt, Casp3, CD4, TGF-­β and Couto et al. (2015)
TNF-­α, IL-­1b
Turbot
9.18 ± 0.02 g Nucleotide supplementation on SBM 60 days In 00.3 g kg−1, 1 g kg−1 nucleotide, 400 g kg−1, 500 g kg−1 SBM Peng et al. (2013)
↑ respiratory burst activity in 0.3 g kg−1 nucleotide, 300 g kg−1 SBM
↑ lysozyme activity in 500 g kg−1 SBM
↓ lysozyme activity
Senegalese sole
3.5 ± 0.2 g 100% FO replacement by SBO or LO 90 days No changes in survival rate Montero et al. (2015)
↑ complement-­related genes
↑ IL-­1b, IL-­10, IL-­11a, IL-­12b, IL-­17c
↑ TLR1, TLR9, IL1RL1, CXCR2, CD4 lysozyme, IRFs
↑ Differentiation antigens and antiviral defence-­related genes
↓ immune-­related genes upon stress
Tilapia
0.15 ± 0.005 g 480 and 600 mg/kg nucleotide inclusion in 10 weeks ↑ Serum lysozyme activity Shiau et al. (2015)
low fish meal (60 g kg−1) and high SBM ↑ Leucocyte activation by ConA and PHA-­P stimulation
(560 g kg−1) ↑ Survival upon S. iniae challenge
5.2 g 700 g kg−1 SBM and 300 g kg−1 RSM 8 weeks → No adverse effects on innate immune response and resistance to Deng et al. (2015)
A. hydrophila
Channel catfish
6.15 ± 0.05 500 g kg−1 SBM and 500 g kg−1 CSM 10 weeks ↑ Macrophage chemotaxis Barros et al. (2002)
↑ Agglutinating antibody
↑ Survival upon E. ictaluri challenge
Red drum
10.9 ± 0.2 500 g kg−1 SBM and 500 g kg−1 FM with FOS, 4 weeks ↑ Serum lysozyme Buentello et al. (2010)
MOS, or TOS (10 g kg−1). ↑ Intracellular superoxide anion
↑ Survival upon A. ocellatum
10.9 ± 0.2 400 g kg−1 SBM 15 weeks → non-­specific immunity parameters evaluated Rossi, Tomasso, and
Gatlin (2015)
Amberjack
25.05 ± 0.1 g 150 g kg−1 and 300 g kg−1 SBM with 56 days ↑ Lysozyme and bactericidal activity Dawood et al. (2015)
heat-­killed L. plantarum
Cambaridae
(15.68 ± 1.06 g) Increased ratio of FM:SBM from 1:1 to 1:1.5 100 days ↓ Superoxide dismutase activity and malondialdehyde levels Wang et al. (2012)
|

(Continues)
      655
 |
656       ZHOU et  al

4.1.2 | Rainbow Trout

Chen et al. (2016)

Ding et al. (2015)
Rumsey et al. (1994) reported that rainbow trout fed SBM for

Cai et al. (2014)

26 weeks showed increased leucocyte cell numbers, plasma proteins

References
and antibody concentration. In addition, the activities of neutro-
phil, monocytes and macrophage were increased as well. However,
Burrells, Williams, Southgate, and Crampton (1999) indicated that if
SBM was replaced by more than 60%–70% of FM, which was compa-
rable to 200 g kg−1–300 g kg−1 inclusion in diets, the suppression of

↓ superoxide dismutase, malondialdehyde, phenoloxidase, acid

innate immune capacity was evident. Jalili, Tukmechi, Agh, Noori, and
Ghasemi (2013) prepared a mixture of plant protein source containing
↓ Hemocyte count and haemolymph phagocytic activity

wheat gluten, corn gluten and SBM (25% of the total plant protein
No changes in serum lysozyme activity and survival

phosphatase, alkaline phosphatase and lysozyme mixture). Juvenile rainbow trout fed the mixture replaced 40% of FM
showed no noticeable negative effects in both total serum antibodies
and alterative complement activity. Deng, Kang, Tao, Rong, and Zhang
(2013) studied the effect of dietary cholesterol included in SBM-­based
Results by feeding SBM/SPC/SBO

diets. In this study, rainbow trout, average weight of 57.8 g, were fed
for 9 weeks with SBM-­based diets (replaced 70% of FM) containing
graded levels of cholesterol. Fish fed diets supplemented with 0.9 or
12 g kg−1 cholesterol increased various innate immune parameters
such as respiratory burst activity, alternative complement activity,
serum and hepatic lysozyme activities, and phagocytic activity. These
elevated innate immune responses induced by cholesterol in fish fed
the SBM-­based diets correlated with the enhanced survival rates upon
challenge with a pathogen, Aeromonas hydrophila. However, when the
level of cholesterol supplementation was increased to more than 12
g kg−1 in the diets, the innate immune parameters declined along with
the survival rates postchallenge.
Length of adm.

14 weeks
10 weeks
8 weeks

FOS, fructooligosaccharide; MOS, mannan-­oligosaccharide; TOS, transgalactooligosaccharide.

4.2 | Sparidae

4.2.1 | Gilthead Sea Bream (Sparus aurata L.)

Montero et al. (2008) investigated the dietary effect of a vegetable oil
Fermented SBM replacement 25, 50, 75,

mixture of SBO and FO at an equal ratio on gilthead sea bream. Fish

fed the vegetable mixture in diets showed significantly reduced levels
400 g kg−1 and 600 g kg−1 SBM

of phagocytic activity and alternative complement pathway activity.

In a later study, juvenile gilthead sea bream were fed 80 days on a diet
where the FO was totally (100%) or partially (70%) replaced by SBO
(Montero et al., 2010). Gilthead sea bream fed the SBO diet displayed
Soybean product

increased expression of proinflammatory cytokines in the intestine

such as TNF-­α and IL-­1b. Furthermore, these fish were more suscepti-
60 g SBO
100%

ble to the pathogen when challenged with Flavobacterium psychrophi-

↑, increase; →, no change; ↓, decrease.

lum. Kokou, Rigos, Henry, Kentouri, and Alexis (2012) evaluated the
effects of SBM when it was used as a protein source in diets. Juvenile
gilthead sea breams that were fed the SBM-­containing diet (20% and
T A B L E   6   (Continued)

40% replacement) for 3 months exhibited significant decrease in their

blood respiratory burst activity. Respiratory burst is an indication of
Fish species/weight

Chinese mitten crab

0.103 ± 0.0009 g

the active state of blood innate immune cells leading to microbicidal

1.48 ± 0.04 g
2.35 ± 0.14 g

activity. In contrast, serum myeloperoxidase activity and bacterio-

lytic activity of complement were significantly increased in the group
Prawns

that was fed a diet of 60% SBM replacement. Myeloperoxidase is

produced mainly by neutrophils and carry out antimicrobial activity
ZHOU et  al
through synthesizing hypohalous acids (Klebanoff, 2005). In a similar
study with an increased feeding period up to 6 months, only the fish
that were fed 40% SBM replacement displayed an increase in serum
respiratory burst activity, whereas the 60% SBM diet-­fed group dis-
played signs of intestinal inflammation (Kokou et al., 2015).
Costas et al. (2014) evaluated the effects of two purified antinu-
trients, soy saponins and phytosterols alone or in combination, on the
immunomodulation of gilthead seabream. The results showed that
plasma bactericidal and alternative complement pathway activities in-
creased in fish fed antinutrients compared to fish fed the control diet
during the course of the experiment with more important changes at 7
and 48 days for bactericidal activity and at 7 and 15 days for comple-
ment values. To our knowledge, this is the first evidence that dietary
purified saponins and phytosterols differentially stimulate the fish im-
mune system.
4.3 | Cyprinidae
4.3.1 | Zebrafish (Danio rerio)
In the resent study of Fuentes-­Appelgren et al. (2014), zebrafish were
used as a model to evaluate the effects of diets supplemented with
SBM components, such as saponins and soy protein on the innate im-
mune system. A significant increase in the number of granulocytes
was observed after feeding fish diets containing high saponin or soy
protein contents. These dietary components also induced the expres-
sion of genes related to the innate immune system, including myeloid-­
specific peroxidase, as well as the complement protein and cytokines.
These results indicate that both soy saponins and proteins may play
roles in the induction of the inflammatory signals that lead to enteritis
in the gut of fish when high levels of these components are incorpo-
rated into the diet.
4.4 | Perciformes
4.4.1 | Japanese Sea Bass (Lateolabrax japonicus)
Juvenile Japanese sea bass were fed for 66 days with a diet in which
FO was replaced with SBO or linseed oil (LO) in different ratios (Xu
et al., 2015). However, supplementations with both SBO and LO did
not reduce the specific growth rate, but showed reduced innate im-
mune responses: phagocytic index; respiratory burst; lysozyme ac-
tivity; and the alternative complement pathway. Lysozyme and the
alterative complement system play a role in bacteria killing.
4.5 | Moronidae
4.5.1 | European Sea Bass (Dicentrarchus labrax)
−1
Effects of 0.4 g kg inclusion of mannan-­oligosaccharide (MOS) in
SBO-­supplemented diets were assessed in juvenile European sea bass
(Torrecillas et al., 2015). Following 8 weeks of feeding with the MOS-­
containing diet, the authors analysed the transcriptomic profiles of the
|
      657
intestinal tissue. When fish were fed with an SBO-­based diet without
MOS, they showed downregulated gene expressions of TCRβ, COX2,
IL-­1β, TNF-­α, IL-­8, IL-­6, IL-­10, TGF-­β, and Ig and upregulated MHCII
expression. However, when MOS was supplemented to the same
SBO-­based diets, the fish showed upregulation of IL-­6, TGF-­β and
IL-­10. It appears that the inclusion of MOS partially counterbalanced
the immunologically negative effects of the SBO diets. Couto et al.
(2015) tested the dietary effects of soy saponins on European sea bass
(283 g) for 59 days. Fish were fed FM and FO-­based diet containing
different levels of soy saponins (1 and 2 g/kg) or a mixture of soy
saponins and phytosterols. Gene expression of immune-­related genes
was studied in addition to histological studies and digestion-­related
enzymatic activities in distal intestine samples. The authors revealed
no overt differences in the expression of immune-­related between the
groups and the fish showed high tolerance to dietary ANFs.
4.6 | Scophthalmidae
4.6.1 | Turbot (Scophthalmus maximus L.)
Nucleotides were added to an SBM-­supplemented diet to test whether
nucleotides could counterbalance an unfavourable immunological
status of turbot caused by an SBM-­based diet (Peng et al., 2013).
Juvenile turbot were fed with conditioned diets for two months: the
diets were supplemented with SBM at various ratios and each diet
included different concentrations of commercially available mixed
nucleotides. The group that were fed the diet containing 0.3 g kg−1
nucleotide significantly increased respiratory burst activity in spite of
the fact that the diet comprised of 400 g kg−1 SBM. Feed solely con-
taining 400 g kg−1 SBM would otherwise decrease respiratory burst.
An increase in lysozyme activity was seen in the fish that were fed a
diet supplemented both 300 g kg−1 of SBM and 0.3 g kg−1 nucleotides.
However, when the proportion of nucleotides was increased up to 1
g kg−1, lysozyme activity decreased down to a comparable level of the
control group.
4.7 | Soleidae
4.7.1 | Senegalese Sole (Solea senegalensis)
The dietary effects of SBO and LO were studied by supplementing
in a fish diet (560 g kg−1 crude protein and 120 g kg−1 crude lipid)
(Montero et al., 2015). Senegalese sole juveniles (3.5 ± 0.2 g) were fed
for 90 days with a diet-­containing SBO, LO or FO as a lipid source. At
the end of the experimental period, the levels of immune-­related gene
expression in the intestine were examined in addition to assessing
growth, cortisol and intestinal fatty acid composition. Further, a stress
test was performed by net chasing for 5 min. There were no differ-
ences in growth, cortisol and intestinal fatty acid composition among
groups. However, the groups fed with a diet including vegetable oil
showed elevated levels of immune-­associated genes: proinflammatory
cytokine genes (IL-1b, IL-12 and IL-17), pattern recognition receptor
genes (TLR1 and TLR9) and cytokine or chemokine receptor genes
 |
658       ZHOU
(IL-1RL1 and CXCR2). These data suggest that an inclusion of vegeta-
ble oil in diets may induce inflammatory responses in Senegalese sole
intestine. Further when stressed, the fish showed reduced expressions
of those genes.
4.8 | Cichlidae
4.8.1 | Tilapia (Oreochromis niloticus)
Juvenile hybrid tilapia fed with a diet supplemented with nucleotides
in SBM-­based diets for 10 weeks increased serum lysozyme activ-
ity and indexes of leucocyte activation stimulated by Concanavalin
A (ConA) and phytohaemagglutinin (PHA-­P) (Shiau, Gabaudan, & Lin,
2015). Fish fed diet supplemented with <240 mg of nucleotides in
SBM-­based diets (60 g kg−1 and 560 g kg−1 replacement) revealed the
highest immune parameters. These immune parameters correlated
with the survivability from a pathogen challenge with Streptococcus
iniae. Deng, Mai, Chen, Mi, and Zhang (2015) tested the dietary effect
of SBM substituted with 30% of rubber seed meal (RSM). The tilapia
fed the protein mixture showed no adverse effect on innate immune
response and resistance to A. hydrophila challenge.
4.9 | Siluriformes
4.9.1 | Channel Catfish (Ictalurus punctatus)
Barros, Lim, and Klesius (2002) investigated the dietary effect of the
SBM mixed with different proportions of solvent-­extracted CSM. The
channel catfish fed the protein mixture of 500 g kg−1 SBM and 500 g
kg−1 CSM revealed increased levels of macrophage chemotaxis and
agglutinating antibody titre. When challenged with E. ictaluri, mortal-
ity was reduced in the fish fed the protein mixture compared to SBM
alone.
4.10 | Sciaenidae
4.10.1 | Red drum (Sciaenops ocellatus)
Buentello, Neill, and Gatlin (2010) tested the effect of prebi-
otic supplementation in the SBM-­based diet (50% substitution).
Fructooligosaccharide, transgalactooligosaccharide or mannan-­
oligosaccharide (10 g/kg) was added to the SBM-­based diet and fed
red drum for 4 weeks. The fish produced increased levels of both
serum lysozyme and intracellular superoxide anion and were pro-
tected against A. ocellatum exposure.
4.11 | Carangidae
4.11.1 | Amberjack (Seriola dumerili)
Heat-­killed Lactobacillus plantarum (1 g kg−1) were included to SBM-­
based diets to assess its immunological balance effects on juvenile
amberjack during a 56-­day feeding trial (Dawood, Koshio, Ishikawa,
et  al
& Yokoyama, 2015). Juvenile amberjack that were fed with 15 g kg−1
and 300 g kg−1 SBM with heat-­killed Lb. plantarum significantly en-
hanced lysozyme and bactericidal activity.
4.11.2 | Golden Pompano (Trachinotus ovatus)
Juvenile golden pompano fed a diet with 40 mg/kg soybean isofla-
vones (SI) showed significant increase in lysozyme activity as well as
respiratory burst activity, and significant higher postchallenge survival
was observed in fish fed diets with 40–80 mg/kg SI supplement than
that in control group (p < .05). Results indicated that dietary intake
containing SI could enhance the immune ability of fish and improve
its resistance to infection by Vibrio harveyi. So we supposed that SI
can be supplemented in the diet as an immunostimulant to enhance
the non-­specific immune ability of fish and production in fish farming
(Zhou et al., 2015).
4.12 | Palaemonidae
4.12.1 | Freshwater Shrimp (Macrobrachium
nipponense)
Ding et al. evaluated the effects of diets that replaced FM by fer-
mented SBM in juvenile prawns of freshwater shrimp for 8 weeks
(Ding, Zhang, Ye, Du, & Kong, 2015). As the supplementation ratio
of fermented SBM was increased, juvenile prawns displayed a de-
crease in total hemocyte count and haemolymph phagocytic activity.
However, the prawns fed with the fermented SBM-­included diet (250
g kg−1) showed significantly higher weight gain and specific growth
rate than those of other experimental groups and the FM-­fed control
group.
4.13 | Varunidae
4.13.1 | Chinese Mitten Crabs (Eriocheir sinensis)
When juvenile Chinese mitten crabs were fed with a diet-­containing
SBM (400 g kg−1 and 600 g kg−1) for 14 weeks, no changes in serum
lysozyme were detected (Cai et al., 2014). It appeared that the SBM-­
supplemented diet did not cause an adverse effect on the immune
responses of the crabs.
5 | INTERACTIONS BETWEEN THE IMMUNE
RESPONSE AND GUT MICROBIOTA IN FISH
FED SOYBEAN PRODUCTS
Even though some papers addressed the effect of SBM, SPC and SO
on the gut microbiota of fish, further investigations are needed, as
the intestinal microbiota influence: development, digestion, nutri-
tion, immunological functions and disease resistance (Montalban-­
Arques et al., 2015; Romero, Ringø, & Merrifield, 2014). According to
Purchiaroni et al. (2013), the gut microbiota together with digestive
ZHOU et  al
enzymes, mucins, peristalsis, epithelial barrier with tight junctions
belongs to the so-­called non-­immune component of mucosal immu-
nity. Furthermore, the importance of the intestinal microbiota is the
discovery that it is required for full immune maturation (Chung et al.,
2012; Kamada, Seo, Chen, & Núnez, 2013) and responsibility of in-
flammatory diseases (Kamada et al., 2013; Rendueles et al., 2012), and
it may also increase the host’s resistance towards pathogenic invasion
and infection (De Schryver & Vadstein, 2014). In addition, the micro-
organisms within the GI tract play important roles in the hosts normal
development and tissue physiology (Bates et al., 2006).
Information is available revealing that soy saponins induce enteri-
tis in Atlantic salmon (Chikwati et al., 2012; Knudsen, Urán, Arnous,
Koppe, & Frøkiær, 2007; Knudsen et al., 2008; Krogdahl et al., 2015), in
contrast to gilthead sea bream and European sea bass where dietary sa-
ponins did not affect intestinal morphology (Couto et al., 2014, 2015).
A controversial hypothesis is the induced enteritis due to saponins and/
or to the gut microbiota; as it is well known that gut bacteria promote
intestinal inflammation (e.g., Ding et al., 2010; Peek & Blaser, 1996; Yan,
Yang, & Ji, 2009). However, to the author’s knowledge, no information
is available on the effect of soy saponins on gut microbiota in salmo-
nids, in contrast to that reported for other sources of saponins on gut
microbiota of endothermic animals (Chen, Tai, & Hsiao, 2015; Gong,
Xiao, Wang, & Yang, 2014; Juan, Zhang, Wang, An, & Wang, 2013; Wan
et al., 2013; Zhang, Xie, Zhang, & Zhang, 2014). However, it is revealed
that SBMIE lead to modulation of the Atlantic salmon gut microbi-
ota (Reveco et al., 2014) and bacterial DNA in rainbow trout plasma
(Mosberian-­Tanha et al., 2016), as well as oxazole-­induced enteritis in
zebrafish modulate the gut microbiota (Brugman et al., 2009). When
discussing enteritis, it is worth to mention that Vasanth et al. (2015)
®
revealed that a microbial feed additive (Bactocell ) abates intestinal in-
flammation in Atlantic salmon, while in zebrafish dietary lactoferrin acts
as an intestinal anti-­inflammatory agent and improved performance
against Edwardsiella tarda (Ulloa et al., 2016). In contrast, Sealey, Conley,
and Bensley (2015) reported marginal effects of prebiotic (Grobiotic-­A)
supplementation on growth performance, intestinal health and disease
resistance towards Flavobacterium psychrophilum of Westslope cut-
throat trout (Oncorhynchus clarkia) fed 300 g kg−1 SBM. It is also worth
to mention that Cohen and Shai (2014) revealed reduction of inflamma-
tion by neutralization of endotoxin by antimicrobial peptides.
Another topic deserving attention is microbial degradation of an-
tinutritional factors and genetically modified plants by the fish intesti-
nal microbiota as no information is available (Ringø et al., 2016). When
discussing microbial degradation of ANFs, it is worth to mention that
the gut microbiota differs between genders in endothermic animals
(Bolnick et al., 2014; Deusch et al., 2015; Mueller et al., 2006; Shastri,
McCarville, Kalmokoff, Brooks, & Green-­Johnson, 2015; Zwielehner
et al., 2011) as well as aquatic animals (Iehata et al., 2015; Li et al.,
2016). Based on this fact, a controversial hypothesis can be put for-
ward. Does this difference in gut microbiota have any influence on
degradation of ANFs?
Several studies have focused on ways to complement the immu-
nologically adverse effects of SBM-­based or SO-­containing fish diets.
These approaches were to supplement those diets with cholesterol
|
      659
(Deng et al., 2013) or various kinds of immunostimulants, such as
MOS (Torrecillas et al., 2015), heat-­killed Lb. plantarum (Dawood et al.,
2015) and nucleotides (Peng et al., 2013; Shiau et al., 2015). These
studies collectively suggest that the inclusion of immunostimulants
in SBM-­based diets helped counterbalance unfavourable innate im-
mune responses. However, the mechanism of these actions is unclear.
For example, research has hypothesized that the effects of MOS may
be related to increase the goblet (mucous producing) cell density and
the mucous cell area in the posterior gut and partially compensating
the downregulation caused by SBO in the expression of certain genes
such as IL-­6, IL-­10 and TGF-­β, which are related to the functioning of
the mucous barrier and maintain immune homoeostasis. As the mode
of action is not clarified, further evaluation and optimization of immu-
nostimulants are needed and the combined effects of MOS and SBO
on the intestinal microbiota and intestinal histology.
Some probiotic studies indicate that individual probiotics induced
specific types of cytokines in fish (B. Beck & S.K. Song, unpublished
data): some induced proinflammatory cytokines, while others induced
anti-­inflammatory cytokines. Inclusion of probiotic may be a possible
alternative to neutralize the negative effects of SBM-­based diets of
SO-­containing feed. However, Sealey, Barrows, Smith, Overturf, and
La Patra (2009) revealed no detectable benefit of probiotic, Mycolator
Dry Probiotic®, in rainbow trout fed 200 g kg−1 SBM on gut health or
intestinal TNF-­α expression.
Recently, SBM utilized as a protein source in fish diets has been ex-
panded its applicability to diets for cambaridae (Wang, Wang, & Wang,
2012), shrimp (Ding et al., 2015) and crab (Cai et al., 2014). However,
more studies on the effect on gut microbiota and innate immune sys-
tem are required for further confirmation of the usability of SBM.
6 | CONCLUSIONS
Using plant-­based raw materials may have both advantages and dis-
advantages. Firstly, imbalanced plant-­based diets and noxious com-
pounds such as antinutrients may impair fish immunity, maturation
and functionality of the intestinal mucosa, the first line of defence
and in particular damage the GI tract which is a port of entry for many
pathogenic agents. Furthermore, endothermic and fish studies have
shown atrophy of intestinal mucosa and a reduction in its absorptive
and immunological capacity in response to high dietary SBM inclusion.
Secondly, using the correct mixture of plant-­based additives provides
not only the option of limiting harm, but also there is also an interest-
ing possibility to enhance GI immunity and disease resistance. All the
immunological studies cited in the present review revealed a list of im-
mune parameters at a specific point in time after treatment. However,
immune parameter(s) directly responsible for disease protection was
not specified. Further studies should therefore be extended to under-
stand the underlying mechanism of prophylactic responses. In addi-
tion, the anaphylactic effects of both SBM and SBO and the immune
regulatory mechanisms involved merits further investigation.
However, based on the likelihood that future carnivorous aqua-
culture will have to rely on plant-­based raw materials, it is strongly
 |
660       ZHOU
recommended that these topics should be given high priority in the
years to come. Readers with special interest in the use of plant prod-
ucts in aquaculture are referred to the reviews of Gatlin et al. (2007),
Bakke-­McKellep and Refstie (2008); Barrows et al. (2008), Ringø and
Olsen (2008), Hemre et al. (2009), Krogdahl et al. (2010), Hansen and
Hemre (2013) and Newaj-­Fyzul and Austin (2015). Furthermore, as
the present review does not focus on soybean lecithin, readers with
special interest are referred to the highly cited review of Coutteau,
Geurden, Camara, Bergot, and Sorgeloos (1997).
ACKNOWLE DG E MEN T
National Research Foundation of Korea (NRF-­2014R1A2A1A11051899,
NRF-­2015R1D1A1A01056959) supports S.K.S.
REFERENCES
Anderson, R. L., & Wolf, W. J. (1995). Compositional changes in trypsin
inhibitors, phytic acid, saponins and isoflavones related to soybean
processing. Journal of Nutrition, 125, 581S–588S.
Ari, M. M., Ayanwwale, B. A., Adama, T. Z., & Olatunji, E. A. (2012).
Evaluation of the chemical composition and anti nutritional factors
(ANFs) levels of different thermally processed soybeans. Asian Journal
of Agricultural Research, 6, 91–98.
Baeverfjord, G., & Krogdahl, A. (1996). Development and regression of soy-
bean meal induced enteritis in Atlantic salmon, Salmo salar L., distal
intestine: A comparison with the intestines of fasted fish. Journal of Fish
Diseases, 19, 375–387.
Bakke-McKellep, A. M., Froystad, M. K., Lilleeng, E., Dapra, F., Refstie, S.,
Krogdahl, A., & Landsverk, T. (2007). Response to soy: T-­cell-­like reac-
tivity in the intestine of Atlantic salmon, Salmo salar L.. Journal of Fish
Diseases, 30, 13–25.
Bakke-McKellep, A. M., Koppang, E. O., Gunnes, G., Sanden, M., Hemre,
G. I., Landsverk, T., & Krogdahl, A. (2007). Histological, digestive,
metabolic, hormonal and some immune factor responses in Atlantic
salmon, Salmo salar L., fed genetically modified soybeans. Journal of
Fish Diseases, 30, 65–79.
Bakke-McKellep, A. M., Penn, M. H., Salas, P. M., Refstie, S., Sperstad, S.,
Landsverk, T., … Krogdahl, Å. (2007). Effects of dietary soybean meal, in-
ulin and oxytetracycline on gastrointestinal histological characteristics,
distal intestine cell proliferation and intestinal microbiota in Atlantic
salmon (Salmo salar L.). British Journal of Nutrition, 97, 699–713.
Bakke-McKellep, A. M., Press, C. M., Baeverfjord, G., Krogdahl, A., &
Landsverk, T. (2000). Changes in immune and enzyme histochemical
phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo
salar L., with soybean meal-­induced enteritis. Journal of Fish Diseases,
23, 115–127.
Bakke-McKellep, A. M., & Refstie, S. (2008). Alternative protein sources
and digestive function alterations in teleost fishes. In J. E. P. Cyrino, R.
Roubach, D. Bureau, & B. G. Kapoor (Eds.), Feeding and digestive func-
tions of fishes (pp. 440–472). Enfield, NH: Science Publishers Inc.
Bansal, T., Alaniz, R. C., Wood, T. K., & Jayaraman, A. (2010). The bacte-
rial signal indole increases epithelial-­cell tight-­junction resistance
and attenuates indicators of inflammation. Proceedings of the National
Academy of Sciences, 107, 228–233.
Barros, M. M., Lim, C., & Klesius, P. H. (2002). Effect of soybean meal re-
placement by cottonseed meal and iron supplementation on growth,
immune response and resistance of channel catfish (Ictalurus puctatus)
to Edwardsiella ictaluri challenge. Aquaculture, 207, 263–279.
Barrows, F. T., Bellis, D., Krogdahl, Å., Silverstein, J. F., Herman, E. M.,
Sealey, W. M., … Gatlin, D. M. III (2008). Report of the plant products
et  al
in aquafeed strategic planning workshop 1: An integrated, interdisci-
plinary research roadmap for increasing utilization of plant feedstuffs
in diets for carnivorous fish. Reviews in Fisheries Science, 16, 449–455.
Bates, J. M., Mittge, E., Kuhlman, J., Baden, K. N., Cheesman, S. E., &
Guillemin, K. (2006). Distinct signals from the microbiota promote dif-
ferent aspects of zebrafish gut differentiation. Developmental Biology,
297, 374–386.
Bendiksen, E. Å., Johnsen, C. A., Olsen, H. J., & Jobling, M. (2011).
Sustainable aquafeeds: Progress towards reduced reliance upon ma-
rine ingredients in diets for farmed Atlantic salmon (Salmo salar L.).
Aquaculture, 314, 132–139.
Birkbeck, T. H., & Ringø, E. (2005). Pathogenesis and the gastrointestinal
tract of growing fish. In W. Holzapfel, & P. Naughton (Eds.), Microbial
ecology in growing animals (pp. 208–234). Edinburgh, UK: Elsevier.
Bøgwald, J., & Dalmo, R. A. (2014). Gastrointestinal pathogenesis and
aquatic animals. In D. Merrifield, & E. Ringø (Eds.), Aquaculture nutrition:
Gut health, probiotics and prebiotics (pp. 53–74). Oxford, UK: Wiley-
Blackwell Publishing.
Bolnick, D. I., Snowberg, L. K., Hirsch, P. E., Lauber, C. L., Org, E., Parks, B., …
Svanbäck, R. (2014). Individual diet has sex dependent effects on ver-
tebrate gut microbiota. Nature Communications, 5, 4500. doi:10.1038/
ncomms5500
Brugman, S., Liu, K.-Y., Lindenbergh-Kortleve, D., Samson, J. N., Furuta, G.
T., Renshaw, S. A., … Nieuwenhuis, E. E. S. (2009). Oxazolone-­induced
enterocolitis in zebrafish depends on the composition of the intestinal
microbiota. Gastroenterology, 137, 1757–1767.
Buentello, J. A., Neill, W. H., & Gatlin, D. M. III (2010). Effects of dietary
prebiotics on the growth, feed efficiency and non-­specific immunity
of juvenile red drum Sciaenops ocellatus fed soybean-­based diets.
Aquaculture Research, 41, 411–418.
Burr, G. S., Wolters, W. R., Barrows, F. T., & Hardy, R. W. (2012). Replacing
fishmeal with blends of alternative proteins on growth performance of
rainbow trout (Oncorhynchus mykiss), and early or late stage juvenile
Atlantic salmon (Salmo salar). Aquaculture, 334–337, 110–116.
Burrells, C., Williams, P. D., Southgate, P. J., & Crampton, V. O. (1999).
Immunological, physiological and pathological responses of rainbow
trout (Oncorhynchus mykiss) to increasing dietary concentrations of
soybean proteins. Veterinary Immunology and Immunopathology, 72,
277–288.
Cai, C.-F., Wang, W.-J., Ye, Y.-T., Krogdahl, Å., Wang, Y.-L., Xia, Y.-M., & Yang,
C.-G. (2012). Effect of soybean meal, raffinose and stachyose on the
growth, body composition, intestinal morphology and intestinal micro-
flora of juvenile allogynogenetic silver crucian carp (Carassius auratus ♀
x Cyprinus carpio ♂). Aquaculture Research, 43, 128–138.
Cai, C., Wu, P., Ye, Y., Song, L., Hooft, J., Yang, C., … Wang, Y. (2014).
Assessment of the feasibility of including high levels of oilseed meals in
the diets of juvenile Chinese mitten crabs (Eriocheir sinensis): Effects on
growth, non-­specific immunity, hepatopancreatic function, and intes-
tinal morphology. Animal Feed Science and Technology, 196, 117–127.
Cervantes-Pahm, S. K., & Stein, H. H. (2010). Ileal digestibility of amino
acids in conventional, fermented, and enzyme-­treated soybean meal
and in soy protein isolate, fish meal, and casein fed to weanling pigs.
Journal of Animal Science, 88, 2674–2683.
Chen, Y. L., Chen, L. Q., Qin, J. G., Ding, Z. L., Li, M., Jiang, H. B., … Li, E. C.
(2016). Growth and immune response of Chinese mitten crab (Eriocheir
sinensis) fed diets containing different lipid sources. Aquaculture
Research, 47, 1984–1995.
Chen, L., Tai, W. C. S., & Hsiao, W. L. W. (2015). Dietary saponins from
four popular herbal tea exert prebiotic-­like effects on gut microbiota in
C57BL/6 mice. Journal of Functional Foods, 17, 892–902.
Chen, J., Wang, J., Song, P., & Ma, X. (2014). Determination of glycinin in
soybean and soybean products using a sandwich enzyme-­linked immu-
nosorbent assay. Food Chemistry, 162, 27–33.
Cheung, M. K., Yip, H. Y., Nong, W., Law, P. T. W., Chu, K. H., Kwan, H.
S., & Hui, J. H. L. (2015). Rapid changes of microbiota diversity in the
ZHOU et  al
gut but not the hepatopancreas during gonadal development of the
new shrimp model Neocaridina denticulata. Marine Biotechnology, 17,
811–919.
Chikwati, E. M., Venold, F. F., Penn, M. H., Rohloff, J., Refstie, S., Guttvik,
A., … Krogdahl, Å. (2012). Interactions of soyasaponins with plant in-
gredients in diets for Atlantic salmon, Salmo salar L. British Journal of
Nutrition, 107, 1570–1590.
Chung, H., Pamp, S. J., Hill, J., Surana, N. K., Edelman, S. M., Troy, E. B., …
Kasper, D. L. (2012). Gut immune maturation depends on colonization
with a host-­specific microbiota. Cell, 149, 1578–1593.
Cohen, H., & Shai, Y. (2014). Reduction of inflammation via neutralization
of endotoxin by antimicrobial peptides. Journal of Peptide Science, 20,
S280–S281.
Corr, S. C., Li, Y., Riedel, C. U., O’Toole, P. W., Hill, C., & Gahan, C. G. M.
(2007). Bacteriocin production as a mechanism for the antiinfective
activity of Lactobacillus salivarius UCC118. Proceedings of the National
Academy of Sciences, 104, 7617–7621.
Costas, B., Couto, A., Azeredo, R., Machado, M., Krogdahl, Å., & Oliva-Teles,
A. (2014). Gilthead seabream (Sparus aurata) immune responses are
modulated after feeding with purified antinutrients. Fish & Shellfish
Immunology, 41, 1–10.
Couto, A., Kortner, T. M., Penn, M., Bakke, A. M., Krogdahl, A., & Oliva-Teles,
A. (2014). Effects of dietary soy saponins and phytosterols on gilthead
sea bream (Sparus aurata) during the on-­growing period. Animal Feed
Science and Technology, 198, 203–214.
Couto, A., Kortner, T. M., Penn, M., Bakke, A. M., Krogdahl, Å., & Oliva-Teles,
A. (2015). Dietary saponins and phytosterols do not affect growth, in-
testinal morphology and immune response of on-­growing European
sea bass (Dicentrarchus labrax). Aquaculture Nutrition, 21, 970–982.
Coutteau, P., Geurden, I., Camara, M. R., Bergot, P., & Sorgeloos, P. (1997).
Review on the dietary effects of phospholipids in fish and crustacean
larviculture. Aquaculture, 155, 149–164.
Dawood, M. A., Koshio, S., Ishikawa, M., & Yokoyama, S. (2015). Effects of
partial substitution of fish meal by soybean meal with or without heat-­
killed Lactobacillus plantarum (LP20) on growth performance, digest-
ibility, and immune response of Amberjack, Seriola dumerili juveniles.
BioMed Research International, 2015, 1–11.
De Schryver, P., & Vadstein, O. (2014). Ecological theory as a founda-
tion to control pathogenic invasion in aquaculture. ISME Journal, 8,
2360–2368.
Deng, J., Kang, B., Tao, L., Rong, H., & Zhang, X. (2013). Effects of dietary
cholesterol on antioxidant capacity, non-­specific immune response,
and resistance to Aeromonas hydrophila in rainbow trout (Oncorhynchus
mykiss) fed soybean meal-­based diets. Fish & Shellfish Immunology, 34,
324–331.
Deng, J. M., Mai, K. S., Chen, L. Q., Mi, H. F., & Zhang, L. (2015). Effects of
replacing soybean meal with rubber seed meal on growth, antioxidant
capacity, non-­specific immune response, and resistance to Aeromonas
hydrophila in tilapia (Oreochromis niloticus x O. aureus). Fish & Shellfish
Immunology, 44, 436–444.
Desai, A. R., Links, M. G., Collins, S. A., Mansfield, G. S., Drew, M. D., Van
Kessel, A. G., & Hill, J. E. (2012). Effects of plant-­based diets on the dis-
tal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture,
350–353, 134–142.
Deusch, O., O’Flynn, C., Colyer, A., Swanson, K. S., Allaway, D., & Morris, P.
(2015). A longitudinal study on the feline faecal microbiome identifies
changes into early adulthood irrespective of sexual development. PLoS
ONE, 10, e0144881.
Dimitroglou, A., Merrifield, D. L., Carnevali, O., Picchietti, S., Avella, M.,
Daniels, C. L., … Davies, S. J. (2011). Microbial manipulations to im-
prove fish health and production – a Mediterranean perspective. Fish &
Shellfish Immunology, 30, 1–16.
Dimitroglou, A., Merrifield, D. L., Spring, P., Sweetman, J., Moate, R., &
Davies, S. J. (2010). Effects of mannan oligosaccharides (MOS) supple-
mentation on growth performance, feed utilisation, intestinal histology
|
      661
and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture,
300, 182–188.
Ding, S., Chi, M. M., Scull, B. P., Rigby, R., Schwerbrock, N. M. J., Magness,
S., … Lund, P. K. (2010). High-­fat diet: bacteria interactions promote
intestinal inflammation which precedes and correlates with obesity and
insulin resistance in mouse. PLoS ONE, 5, e12191.
Ding, Z., Zhang, Y., Ye, J., Du, Z., & Kong, Y. (2015). An evaluation of replac-
ing fish meal with fermented soybean meal in the diet of Macrobrachium
nipponense: Growth, nonspecific immunity, and resistance to Aeromonas
hydrophila. Fish & Shellfish Immunology, 44, 295–301.
Drew, M. D., Borgeson, T. L., & Thiessen, D. L. (2007). A review of process-
ing of feed ingredients to enhance diet digestibility in finfish. Animal
Feed Science and Technology, 138, 118–136.
Duar, R. M., Clark, K. J., Patil, P. B., Hernández, C., Brüning, S., Burkey, T.
E., … Walter, J. (2014). Identification and characterization of intestinal
lactobacilli strains capable of degrading immunotoxic peptides present
in gluten. Journal of Applied Microbiology, 118, 515–527.
El-Shemy, H. A. (2011). Soybean and nutrition. Rijeka, Croatia: InTech. ISBN
978-953-307-536-5.
Feedstuffs (2016) Feedstuffs Reference Issue & Buyers Guide 2016.
Retrieved from http://feedstuffs.com/story-feedstuffs-reference-issue-
2016-46-70391
FishBase (2015) Version (10/2015). Retrieved from http://www.fishbase.
org
Food and Agriculture Organization (FAO) (2002) Soybeans: Post-harvest
Operations, Food and Agriculture Organization of the United Nations
pp 94. FI Institutional Websites. In: FAO Fisheries and Aquaculture
Department [online]. Retrieved from http://www.fao.org/fishery/figis/en”
Food and Agriculture Organization (FAO) (2009). The state of world fisheries
and aquaculture 2008. Rome: Food and Agriculture Organization.
Food and Agriculture Organization (FAO) (2016). The state of world fisheries
and aquaculture 2016. Contributing to food security and nutrition for all.
Rome: Food and Agriculture Organization (FAO). 200 pp.
Francis, G., Makkara, H. P. S., & Becker, K. (2001). Antinutritional factors
present in plant derived alternate fish feed ingredients and their effects
in fish. Aquaculture, 199, 197–227.
Fuentes-Appelgren, P., Opazo, R., Barros, L., Feijoo′, C. G., Urzu′a, V., &
Romero, J. (2014). Effect of the dietary inclusion of soybean com-
ponents on the innate immune system in zebrafish. Zebrafish, 11,
41–49.
Ganguly, S., & Prasad, A. (2012). Microflora in fish digestive tract plays
significant role in digestion and metabolism: A review. Review in Fish
Biology and Fisheries, 22, 11–16.
Gatlin, D. M. III, Barrows, F., Brown, P., Dabrowski, K., Gaylord, T. G., Hardy,
R. W., … Wurtele, E. (2007). Expanding the utilization of sustainable
plant products in aquafeeds: A review. Aquaculture Research, 38,
551–579.
Gaylord, T. G., & Barrows, F. T. (2009). Multiple amino acid supplementation
to reduce dietary protein in plant-­based rainbow trout, Oncorhynchus
mykiss, feeds. Aquaculture, 287, 180–184.
Ghanbari, M., Kneifel, W., & Doming, K. J. (2015). A new view of the fish gut
microbiome: Advances from next-­generation sequencing. Aquaculture,
448, 464–475.
Goebel, K. P., & Stein, H. H. (2011). Phosphorus digestibility and energy
concentration of enzyme-­treated and conventional soybean meal fed
to weanling pigs. Journal of Animal Science, 89, 764–772.
Gong, C.-Y., Xiao, W., Wang, Z.-Z., & Yang, Z.-G. (2014). Stability of akebia
saponin D in gastrointestinal contents of rats. China Journal of Chinese
Materia Medica, 39, 2311–2313.
Green, T. J., Smullen, R., & Barnes, A. C. (2013). Dietary soybean protein
concentrate-­induced intestinal disorder in marine farmed Atlantic
salmon, Salmo salar is associated with alterations in gut microbiota.
Veterinary Microbiology, 166, 286–292.
Groff, J., & LaPatra, S. (2000). Infectious diseases impacting the commercial
culture of salmonids. Journal of Applied Aquaculture, 10, 17–90.
 |
662       ZHOU
Hansen, A.-C., & Hemre, G.-I. (2013). Effect of replacing fish meal and oil
with plant resources in on-­growing diets for Atlantic cod Gadus morhua
L. Aquaculture Nutrition, 19, 641–650.
Harikrishnan, R., & Balasundaram, C. (2005). Modern trends in Aeromonas
hydrophila disease management with fish. Reviews in Fisheries Science,
13, 281–320.
Harishankar, M. K., Sasikala, C., & Ramya, M. (2013). Efficiency of the in-
testinal bacteria in degradation of the toxic pesticide, chlorpyrifos.
Biotech, 3, 137–142.
Hartviksen, M., Gonzalez Vecino, J. L., Ringø, E., Bakke, A.-M., Wadsworth,
S., Krogdahl, Å., … Kettunen, A. (2014). Alternative dietary protein
sources for Atlantic salmon (Salmo salar L.) affect intestinal microbiota,
intestinal and liver histology and growth. Aquaculture Nutrition, 20,
381–398.
Hedrera, M. I., Galdames, J. A., Jimenez-Reyes, M. F., Reyes, A. E., Avendano-
Herrera, R., Romero, J., & Feijoo, C. G. (2013). Soybean meal induces
intestinal inflammation in zebrafish larvae. PLoS ONE, 8, 10.
Hei, W., Li, Z., Ma, X., & He, P. (2012). Determination of beta-­conglycinin in
soybean and soybean products using a sandwich enzyme-­linked immu-
nosorbent assay. Analytica Chimica Acta, 734, 62–68.
Heikkinen, J., Vielma, J., Kemilainen, O., Tiirola, M., Eskelinen, P., Kiuru,
T., Navia-Paldanius, D., & von Wright, A. (2006). Effects of soybean
meal based diet on growth performance, gut histopathology and in-
testinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss).
Aquaculture, 261, 259–268.
Hemre, G-I., Amlund, H., Aursand, M., Bakke, A.M., Olsen, R.E., Ringø, E.,
& Svihus, B. (2009) Criteria for safe use of plant ingredients in diets
for aquacultured fish. ISNB 978-82-8082-299-4. Norwegian Scientific
Committee for Food Safety, Oslo, Norway. 173 p. The report is Retrieved
from http://www.vkm.no. ISBN 978-82-8082-299-4 (electronic version).
Herzog Möller. Petfood. Modern soy proteins perfect. Feed Tech 6.3 –
www.AgriWorld.nl, 28-30.
Holtug, K., Rasmussen, H., & Mortensen, P. (1988). Short chain fatty acids
in inflammatory bowel disease. The effect of bacterial fermentation of
blood. Scandinavian Journal of Clinical and Laboratory Investigation, 48,
667–671.
Hong, K.-J., Lee, C.-H., & Kim, S. W. (2004). Aspergillus oryzae GB-­107 fer-
mentation improves nutritional quality of food soybeans and feed soy-
bean meals. Journal of Medicinal Food, 7, 430–435.
Hoseinifar, S. H., Mirvaghefi, A., Amoozegar, M. A., Merrifield, D., & Ringø,
E. (2017). In vitro selection of a synbiotic and in vivo evaluation on
intestinal microbiota, performance and physiological response of rain-
bow trout (Oncorhynchus mykiss) fingerlings. Aquaculture Nutrition, 23,
111–118.
Huang, G. (2008) The study of intestinal bacterial molecular ecology of
cultured fishes. Master thesis, Huazhong Agricultural University (in
Chinese).
Iehata, S., Valenzuela, F., & Riquelme, C. (2015). Analysis of bacterial com-
munity and bacterial nutritional enzyme activity associated with the
digestive tract of wild Chilean octopus (Octopus mimus Gould, 1852).
Aquaculture Research, 46, 861–873.
Jalili, R., Tukmechi, A., Agh, N., Noori, F., & Ghasemi, A. (2013). Replacement
of dietary fish meal with plant sources in rainbow trout (Oncorhynchus
mykiss); effect on growth performance, immune responses, blood in-
dices and disease resistance. Iranian Journal of Fisheries Sciences, 12,
577–591.
Jankowski, J., Juskiewicz, J., Gulewicz, K., Lecewicz, A., Slominski, B. A.,
& Zdunczyk, Z. (2009). The effect of diets containing soybean meal,
soybean protein concentrate, and soybean protein isolate of different
oligosaccharide content on growth performance and gut function of
young turkeys. Poultry Science, 88, 2132–2140.
Juan, X., Zhang, Y.-F., Wang, Y., An, R., & Wang, X.-H. (2013). Study of effect
of different compatibility of saponins contained in banxia xiexin tang
on intestinal bacterium metabolism. China Journal of Chinese Materia
Medica, 38, 611–617.
et  al
Kamada, N., Seo, S.-U., Chen, G. Y., & Núnez, G. (2013). Role of the gut
microbiota in immunity and inflammatory disease. Nature Reviews
Immunology, 13, 321–335.
Kihara, M., & Sakata, T. (2002). Production of short-­chain fatty acids and
gas from various oligosaccharides by gut microbes of carp (Cyprinus
carpio L.) in micro-­scale batch culture. Comparative Biochemistry and
Physiology Part A: Molecular & Integrative Physiology, 132, 333–340.
Kim, D., Brunt, J., & Austin, B. (2007). Microbial diversity of intestinal con-
tents and mucus in rainbow trout (Oncorhynchus mykiss). Journal of
Applied Microbiology, 102, 1654–1664.
Kiron, V. (2012). Fish immune system and its nutritional modulation for pre-
ventive health care. Animal Feed Science and Technology, 173, 111–133.
Klebanoff, S. J. (2005). Myeloperoxidase: Friend and foe. Journal of
Leukocyte Biology, 77, 598–625.
Knudsen, D., Jutfelt, F., Sundh, H., Sundell, K., Koppe, W., & Frøkiær, H.
(2008). Dietary soya saponin increase gut permeability and play a key
role in the onset of soyabean-­induced enteritis in Atlantic salmon
(Salmo salar L.). British Journal of Nutrition, 100, 120–129.
Knudsen, D., Urán, P., Arnous, A., Koppe, W., & Frøkiær, H. (2007). Saponin
containing subfractions of soybean molasses induce enteritis in the
distal intestine of Atlantic salmon. Journal of Agricultural and Food
Chemistry, 55, 2261–2267.
Kokou, F., Rigos, G., Henry, M., Kentouri, M., & Alexis, M. (2012). Growth
performance, feed utilization and non-­specific immune response of gil-
thead sea bream (Sparus aurata L.) fed graded levels of a bioprocessed
soybean meal. Aquaculture, 364, 74–81.
Kokou, F., Sarropoulou, E., Cotou, E., Rigos, G., Henry, M., Alexis, M., &
Kentouri, M. (2015). Effects of fish meal replacement by a soybean
protein on growth, histology, selected immune and oxidative status
markers of gilthead sea bream, Sparus aurata. Journal of the World
Aquaculture Society, 46, 115–128.
Krogdahl, A., Bakke-Mckellep, A. M., Roed, K. H., & Baeverfjord, G. (2000).
Feeding Atlantic salmon Salmo salar L. soybean products: Effects on
disease resistance (furunculosis), and lysozyme and IgM levels in the
intestinal mucosa. Aquaculture Nutrition, 6, 77–84.
Krogdahl, Å., Gajardo, K., Kortner, T. M., Penn, M., Gu, M., Berge, G. M.,
& Bakke, A. M. (2015). Soya saponins induce enteritis in Atlantic
salmon (Salmo salar L.). Journal of Agriculture and Food Chemistry, 63,
3887–3902.
Krogdahl, Å., Penn, M., Thorsen, J., Refstie, S., & Bakke, A. M. (2010).
Important antinutrients in plant feedstuffs for aquaculture: An up-
date on recent findings regarding responses in salmonids. Aquaculture
Research, 41, 333–344.
Li, J., Wang, W., Xu, S. X., Magarvey, N. A., & McCormick, J. K. (2011).
Lactobacillus reuteri-­produced cyclic dipeptides quench agr-­mediated
expression of toxic shock syndrome toxin-­1 in staphylococci.
Proceedings of the National Academy of Sciences, 108, 3360–3365.
Li, Z., Xu, L., Liu, W., Liu, Y., Ringø, E., Du, Z., & Zhou, Z. (2015). Protein
replacement in practical diets altered gut allochthonous bacteria
of cultured cyprinid species with different food habits. Aquaculture
International, 23, 913–928.
Li, X., Yan, Q., Ringø, E., Wu, X., He, Y., & Yang, D. (2016). The influence
of weight and gender on intestinal bacterial community of wild large-
mouth bronze gudgeon (Coreius guichenoti, 1874). BMC Microbiology,
16, 191. doi:10.1186/s12866-­016-­0809-­1
Lilleeng, E., Penn, M. H., Haugland, O., Xu, C., Bakke, A. M., Krogdahl, A.,
… Froystad-Saugen, M. K. (2009). Decreased expression of TGF-­beta,
GILT and T-­cell markers in the early stages of soybean enteropathy in
Atlantic salmon (Salmo salar L.). Fish & Shellfish Immunology, 27, 65–72.
Lim, C, Webster, C.D., & Lee, C.-S. (Eds.) (2008) Alternative protein sources in
aquaculture diets (p. 571), New York: The Haworth Press.
Llewellyn, M. S., Boutin, S., Hoseinifar, S. H., & Derome, N. (2014). Teleost
microbiomes: The state of the art in their characterization, manipulation
and importance in aquaculture and fisheries. Frontiers in Microbiology, 5,
207. doi:10.3389/fmicb.2014.00207
ZHOU et  al
Lødemel, J. B., Mayhew, T. M., Myklebust, R., Olsen, R. E., Espelid, S., &
Ringø, E. (2001). Effect of three dietary oils on disease susceptibility
in Arctic charr (Salvelinus alpinus L.) during cohabitant challenge with
Aeromonas salmonicida ssp. salmonicida. Aquaculture Research, 32,
935–945.
Mansfield, G. S., Desai, A. R., Nilson, S. A., Van Kessel, A. G., Drew, M. D.,
& Hill, J. E. (2010). Characterization of rainbow trout (Oncorhynchus
mykiss) intestinal microbiota and inflammatory marker gene expression
in a recirculating aquaculture system. Aquaculture, 307, 95–104.
Marcil, V., Delvin, E., Seidman, E., Poitras, L., Zoltowska, M., Garofalo, C.,
& Levy, E. (2002). Modulation of lipid synthesis, apolipoprotein bio-
genesis, and lipoprotein assembly by butyrate. American Journal of
Physiology. Gastrointestinal and Liver Physiology, 283, G340–G346.
Maslowski, K. M., & Mackay, C. R. (2010). Diet, gut microbiota and immune
responses. Nature Immunology, 12, 5–9.
Médale, F., Boucher, R., DuPont-Nivet, M., Quillet, E., Aubin, J., & Panserat,
S. (2013). Des aliments á base de végétaux pour les poissons délevage.
INRA Productions Animales, 26, 303–316.
Merrifield, D. L., Bradley, G., Baker, R. T. M., Dimitroglou, A., & Davies, S. J.
(2009). Soybean meal alters autochthonous microbial populations, mi-
crovilli morphology and compromises intestinal enterocyte integrity of
rainbow trout (Oncorhynchus mykiss Walbaum). Journal of Fish Diseases,
32, 755–766.
Merrifield, D. L., Dimitroglou, A., Foey, A., Davies, S. J., Baker, R. R., Bøgwald,
J., … Ringø, E. (2010). The current status and future focus of probiotic
and prebiotic applications for salmonids. Aquaculture, 302, 1–18.
Merrifield, D. L., Olsen, R. E., Myklebust, R., & Ringø, E. (2011). Dietary
effect of soybean (Glycine max) products on gut histology and microbi-
ota of fish. In H. El-Shemy (Ed.), Soybean and nutrition (pp. 231–250).
InTech: Rijeka, Croatia. ISBN 978-953-307-536-5.
Merrifield, D. L., & Rodiles, A. (2015). The fish microbiome and its interac-
tions with mucosal tissues. In B. H. Beck, & E. Peatman (Eds.), Mucosal
health in aquaculture (pp. 273–295). Amsterdam: Elsevier.
Metochis, C., Crampton, V. O., Ruohonen, K., Bell, J. G., Adams, A., &
Thompson, K. D. (2016). The effects of increasing dietary levels of
amino acid-­supplemented soy protein concentrate and constant di-
etary supplementation of phosphorus on growth, composition and
immune responses of juvenile Atlantic salmon (Salmo salar L.). Fish
Physiology and Biochemistry, 42, 807–829.
Montalban-Arques, A., De Schryver, P., Bossier, P., Gorkiewicz, G., Mulero,
V., Gatlin, D. M. III, & Galindo-Villegas, J. (2015). Selective manipulation
of the gut microbiota improves immune status in vertebrates. Frontiers
in Immunology, 6, 512. doi:10.3389/fimmu.2015.00512
Montero, D., Benitez-Dorta, V., Caballero, M. J., Ponce, M., Torrecillas,
S., Izquierdo, M., Zamorano, M. J., & Manchado, M. (2015). Dietary
vegetable oils: Effects on the expression of immune-­related genes
in Senegalese sole (Solea senegalensis) intestine. Fish & Shellfish
Immunology, 44, 100–108.
Montero, D., Grasso, V., Izquierdo, M. S., Ganga, R., Real, F., Tort, L., …
Acosta, F. (2008). Total substitution of fish oil by vegetable oils in gil-
thead sea bream (Sparus aurata) diets: Effects on hepatic Mx expres-
sion and some immune parameters. Fish & Shellfish Immunology, 24,
147–155.
Montero, D., Mathlouthi, F., Tort, L., Afonso, J. M., Torrecillas, S., Fernandez-
Vaquero, A., … Izquierdo, M. S. (2010). Replacement of dietary fish oil
by vegetable oils affects humoral immunity and expression of pro-­
inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish
& Shellfish Immunology, 29, 1073–1081.
Mosberian-Tanha, P., Øverland, M., Landsverk, T., Reveco, F. E., Schrama,
J. W., Roem, A. J., … Mydland, L. T. (2016). Bacterial translocation and
in vivo assessment of intestinal barrier permeability in rainbow trout
(Oncorhynchus mykiss) with and without soybean meal-­induced inflam-
mation. Journal of Nutritional Science, 5, e26. doi:10.1017/jns.2016.7
Mueller, S., Saunier, K., Hanisch, C., Norin, E., Alm, L., Midtvedt, T., … Clavel,
T. (2006). Difference in faecal microbiota in different European study
|
      663
populations in relation to age, gender, and country: A cross-­sectional
study. Applied and Environment Microbiology, 72, 1027–1033.
Navarrete, P., Fuentes, P., De la Fuentes, L., Barros, L., Magne, F., Opazo,
R., … Romero, J. (2013). Short-­term effects of dietary soybean meal
and lactic acid bacteria on the intestinal morphology and microbiota of
Atlantic salmon (Salmo salar). Aquaculture Nutrition, 17, 148–156.
Newaj-Fyzul, A., & Austin, B. (2015). Probiotics, immunostimulants,
plant products and oral vaccines, and their role as feed supplements
in the control of bacterial fish diseases. Journal of Fish Diseases, 38,
937–955.
NRC. National Research Council (2012) Nutrient requirements of swine (11th
rev. edn). Washington DC: Natl. Acad. Press.
Oliva-Teles, A. (2012). Nutrition and health of aquaculture fish. Journal of
Fish Diseases, 35, 83–108.
Olsen, R. E., Waagbø, R., Ringø, E., & Lall, S. P. (2010). Alternative marine
lipid resources. In G. M. Turchini, W.-K. Ng, & D. R. Tocher (Eds.), Fish oil
replacement and alternative lipid sources in aquaculture feeds (pp. 267–
324). Taylor & Francis: CRC Press. ISBN 978-1-4398-0862-7.
Peek, R. M. Jr, & Blaser, M. J. (1996). Pathophysiology of Helicobacter pylori-­
induced gastritis and peptic ulcer disease. American Journal of Medicine,
102, 200–207.
Peng, M., Xu, W., Ai, Q., Mai, K., Liufu, Z., & Zhang, K. (2013). Effects of nu-
cleotide supplementation on growth, immune responses and intestinal
morphology in juvenile turbot fed diets with graded levels of soybean
meal (Scophthalmus maximus L.). Aquaculture, 392, 51–58.
Purchiaroni, F., Tortora, A., Gabrielli, M., Bertucci, F., Gigante, G., Ianiro,
G., … Gasbarrini, A. (2013). The role of intestinal microbiota and the
immune system. European Review for Medical and Pharmacological
Sciences, 17, 323–333.
Raggi, T., & Gatlin, D. M. III (2012). Prebiotics have limited effects on nu-
trient digestibility of a diet based on fish meal and soybean meal in
goldfish. North American Journal of Aquaculture, 74, 400–407.
Rawls, J. F., Samuel, B. S., & Gordon, J. I. (2004). Gnotobiotic zebraf-
ish reveal evolutionarily conserved responses to the gut microbiota.
Proceedings of the National Academy of Sciences of the United States of
America, 101, 4596–4601.
Ray, A. K., Ghosh, K., & Ringø, E. (2012). Enzyme-­producing bacteria iso-
lated from fish gut: A review. Aquaculture Nutrition, 18, 465–492.
Refstie, S., Landsverk, T., Ringø, E., Sundby, A., Shearer, K. D., & Krogdahl,
Å. (2006). Digestive capacity, intestinal morphology and microflora of
1-­year and 2-­year old Atlantic cod (Gadus morhua) fed standard or bio-
processed soybean meal. Aquaculture, 261, 269–284.
Rendueles, O., Ferrieres, L., Fretaud, M., Begaud, E., Herbomel, P., Levraud,
J.-P., & Ghigo, J.-M. (2012). A new zebrafish model of oro-­intestinal
pathogen colonization reveals a key role for adhesion in protection by
probiotic bacteria. PloS Path., 8, 7. doi:10.1371/journal.ppat.1002815
Reveco, F. E., Øverland, M., Romarheim, O. H., & Mydland, L. T. (2014).
Intestinal bacterial community structure differs between healthy and
inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture,
420–421, 262–269.
Ringø, E. (1993) Arctic charr, Salvelinus alpinus (L.), reared in fresh and sea
water. An experimental study of lipid digestion and intestinal micro-
flora. Ph.D. thesis, Norwegian College of Fishery Science, University of
Tromsø, Norway.
Ringø, E., & Birkbeck, T. H. (1999). Intestinal microflora of fish larvae and
fry. Aquaculture Research, 30, 773–789.
Ringø, E., Lødemel, J. B., Myklebust, R., Jensen, L., Lund, V., Mayhew, T. M.,
& Olsen, R. E. (2002). Effect of soybean, linseed and marine oils on aer-
obic gut microbiota of Arctic charr Salvelinus alpinus L. before and after
challenge with Aeromonas salmonicida ssp. salmonicida. Aquaculture
Research, 33, 591–606.
Ringø, E., Løvmo, L., Kristiansen, M., Bakken, M., Salinas, I., Myklebust, R.,
Olsen, R. E., & Mayhew, T. M. (2010). Lactic acid bacteria vs. pathogens
in the gastrointestinal tract of fish: A review. Aquaculture Research, 41,
451–467.
 |
664       ZHOU
Ringø, E., Myklebust, R., Mayhew, T. M., & Olsen, R. E. (2007). Bacterial
translocation and pathogenesis in the digestive tract of larvae and fry.
Aquaculture, 268, 251–264.
Ringø, E., & Olsen, R. E. (2008) Gut health in aquatic species. In E. M. Binder
& G. Schatzmayr (Eds.), World nutrition forum the future of animal pro-
duction (pp. 79–105). Nottingham, UK: Nottingham University Press.
ISBN: 978-1-904761-80-8.
Ringø, E., Olsen, R. E., Gifstad, T. Ø., Dalmo, R. A., Amlund, H., Hemre, G.-I.,
& Bakke, A. M. (2010). Prebiotics in aquaculture: A review. Aquaculture
Nutrition, 16, 117–136.
Ringø, E., Olsen, R. E., Mayhew, T. M., & Myklebust, R. (2003). Electron
microscopy of the intestinal microflora of fish. Aquaculture, 227,
395–415.
Ringø, E., Sigmund Sperstad, S., Kraugerud, O. F., & Krogdahl, Å. (2008).
Use of 16S rRNA gene sequencing analysis to characterise culturable
intestinal bacteria in Atlantic salmon (Salmo salar) fed diets with cellu-
lose or non-­starch polysaccharides from soy. Aquaculture Research, 39,
1087–1100.
Ringø, E., Sperstad, S., Myklebust, R., Refstie, S., & Krogdahl, Å. (2006).
Characterisation of the microbiota associated with the intestine of
Atlantic cod (Gadus morhua L.). The effect of fish meal, soybean meal
and a bioprocessed soybean meal. Aquaculture, 261, 829–841.
Ringø, E., Zhou, Z., Gonzalez Vecino, J. L., Wadsworth, S., Romero, J.,
Krogdahl, Å., … Merrifield, D. L. (2016). Effects of dietary compo-
nents on the gut microbiota of aquatic animals: A never-­ending story?
Aquaculture Nutrition, 22, 219–282.
Romero, J., Ringø, E., & Merrifield, D. L. (2014). The gut microbiota of fish.
In D. Merrifield, & E. Ringø (Eds.), Aquaculture nutrition: Gut health,
probiotics and prebiotics (pp. 75–100). Oxford, UK: Wiley-Blackwell
Publishing.
Rossi, W., Tomasso, J. R., & Gatlin, D. M. III (2015). Production performance
and non-­specific immunity of cage-­raised red drum, Sciaenops ocellatus,
fed soybean-­based diets. Aquaculture, 443, 84–89.
Rowland, I. R. (1988). Interactions of the gut microflora and the host in
toxicology. Toxicologic Pathology, 16, 147–153.
Rumsey, G. L., Siwicki, A. K., Anderson, D. P., & Bowser, P. R. (1994). Effect
of soybean protein on serological response, nonspecific defense-­
mechanisms, growth, and protein-­utilization in rainbow-­trout.
Veterinary Immunology and Immunopathology, 41, 323–339.
Sahlmann, C., Sutherland, B. J. G., Kortner, T. M., Koop, B. F., Krogdahl,
Å., & Bakke, A. M. (2013). Early response of gene expression in the
distal intestine of Atlantic salmon (Salmo salar L.) during the develop-
ment of soybean meal induced enteritis. Fish & Shellfish Immunology,
34, 599–609.
Santerre, A., Téllez-Bañuelos, M. S., Casas-Solís, J., Castro-Félix, P., Huízar-
López, M. R., Zaitseva, G. P., … Juárez-Carrillo, E. (2015). Δ6-­fatty acid
desaturase and fatty acid elongase mRNA expression, phagocytic ac-
tivity and weight-­to-­length relationships in channel catfish (Ictalurus
punctatus) fed alternative diets with soy and a probiotic. Genetics and
Molecular Research, 14, 11222–11234.
Sealey, W. M., Barrows, F. T., Smith, C. E., Overturf, K., & La Patra, S. E.
(2009). Soybean meal level and probiotics in the first feeding fry diets
alter the ability of rainbow trout Oncorhynchus mykiss to utilise high
levels of soybean meal during grow-­out. Aquaculture, 293, 195–2013.
Sealey, W. M., Conley, Z. B., & Bensley, M. (2015). Prebiotic supplemen-
tation has only minimal effects on growth efficiency, intestinal health
and disease resistance of Westslope cutthroat trout Oncorhynchus
clarkia lewisi fed 30% soybean meal. Frontiers in Immunology, 6, 396.
doi:10.3389/fimmu.2015.00396
Shastri, P., McCarville, J., Kalmokoff, M., Brooks, S. P. J., & Green-Johnson,
J. M. (2015). Sex differences in gut fermentation and immune param-
eters in rats fed an oligofructose-­supplemented diet. Biology of Sex
Differences, 6, 13. doi:10.1186/s13293-­015-­0031-­0
Shi, A. Q. (2002). Disposal and comprehensive utilization of intestines
waste water. Pollution Control Technologies, 15, 35–36. (in Chinese).
et  al
Shiau, S. Y., Gabaudan, J., & Lin, Y. H. (2015). Dietary nucleotide supple-
mentation enhances immune responses and survival to Streptococcus
iniae in hybrid tilapia fed diet containing low fish meal. Aquaculture
Research, 2, 77–81.
Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama,
H., & Takeda, K. L. (2013). Commensal bacteria-­dependent indole pro-
duction enhances epithelial barrier function in the colon. PLoS ONE, 8,
e80604. doi:10.1371/journal.pone.0080604
Singh, B. K., & Walker, A. (2006). Microbial degradation of organophospho-
rus compounds. FEMS Microbiology Reviews, 30, 428–471.
Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly,
M., … Garrett, W. S. (2013). The microbial metabolites, short-­chain fatty
acids, regulate colonic Treg cell homeostasis. Science, 341, 569–573.
Tamboli, C. P., Neut, C., Desreumaux, P., & Colombel, J. F. (2004). Dysbiosis
as a prerequisite for IBD. Gut, 53, 1057.
Torrecillas, S., Montero, D., Caballero, J. M., Pittman, K. A., Custodio, M.,
Campo, A., … Izquierdo, M. (2015). Dietary mannan oligosaccharides:
Counteracting the side effects of soybean meal oil inclusion on European
sea bass (Dicentrarchus labrax) gut health and skin mucosa mucus produc-
tion? Frontiers in Immunology, 6, 397. doi:10.3389/fimmu.2015.00397
Turroni, F., Ventura, M., Buttó, L. F., Duranti, S., O′Toole, R. W., Motherway,
M. O., & van Sindern, D. (2014). Molecular dialogue between the
human gut microbiota and the host: A Lactobacillus and Bifidobacterium
perspective. Cellular and Molecular Life Sciences, 71, 183–203.
Ulloa, P. E., Solis, C. J., De la Paz, J. F., Alaurent, T. G. S., Caruffo, M.,
Hernandez, A. J., … Feijoo, C. G. (2016). Lactoferrin decreases the intes-
tinal inflammation triggered by a soybean meal-­based diet in zebrafish.
Journal of Immunology Research, 2016, 1–10.
Urán, P. A., Schrama, J. W., Rombout, J. H. W. M., Obach, A., Jensen, L.,
Koppe, W., & Verreth, J. A. J. (2008). Soy bean meal-­induced enteritis in
Atlantic salmon (Salmo salar L.) at different temperatures. Aquaculture
Nutrition, 14, 324–330.
Van den Ingh, T. S. G. A. M., Krogdahl, Å., Olli, J., Hendricks, H. G. C. J. M.,
& Koninkx, J. F. J. G. (1991). Effects of soybean-­containing diets on the
proximal and distal intestine in Atlantic salmon (Salmo salar): A morpho-
logical study. Aquaculture, 94, 297–305.
Vasanth, G., Kiron, V., Kulkarni, A., Dahle, D., Lokesh, J., & Kitani, Y. (2015).
A microbial feed additive abates intestinal inflammation in Atlantic
salmon. Frontiers in Immunology, 6, 409.
Vinolo, M. A., Rodrigues, H. G., Nachbar, R. T., & Curi, R. (2011). Regulation
of inflammation by short chain fatty acids. Nutrients, 3, 858–876.
Wan, J.-Y., Liu, P., Wang, H.-Y., Qi, L.-W., Wang, C.-Z., Li, P., & Yuan, C.-
S. (2013). Biotransformation of metabolic profile of American gin-
seng saponins with human intestinal microflora by liquid chroma-
tography quadrupole time-­of-­flight mass spectrometry. Journal of
Chromatography A, 1286, 83–92.
Wang, T.-T., Wang, M.-Y., & Wang, Y.-F. (2012) Dietary reduction of fish
meal, supplementation of vitamin C and fish oil may promote ovary
maturation by improving digestibility and immunity in Procambarus
clarkii (Crustacea: Decapoda). Aquaculture Research, 43, 1669–1676.
Xiong, J., Dai, W., & Li, C. (2016). Advances, challenges, and directions in
shrimp disease control: The guidelines from an ecological perspective.
Applied Microbiology and Biotechnology, 100, 6947–6954.
Xiong, J., Wang, K., Wu, J., Qiuqian, L., Yang, K., Qian, Y., & Zhang, D. (2015).
Changes in intestinal bacterial communities are closely associated with
shrimp disease severity. Applied Microbiology and Biotechnology, 99,
6911–6919.
Xu, H., Zhang, Y. J., Wang, J., Zuo, R. T., Mai, K. S., & Ai, Q. H. (2015).
Replacement of fish oil with linseed oil or soybean oil in feeds for
Japanese seabass, Lateolabrax japonicus: Effects on growth perfor-
mance, immune response, and tissue fatty acid composition. Journal of
the World Aquaculture Society, 46, 349–362.
Yan, S., Yang, J., & Ji, W-y (2009). Effects of Staphylococcus aureus and cut
size of tracheal stenosis in albino rabbits: And experimental study.
Journal of China Medical University, 38, 50–59.
ZHOU et  al
Young, J. C., Zhou, T., Yu, H., Zhu, H., & Gong, J. (2007). Degradation of
trichothecene mycotoxins by chickens intestinal microbes. Food and
Chemical Toxicology, 45, 136–143.
Ytrestøyl, T., Aas, T. S., & Åsgård, T. (2015). Utilisation of feed resources
in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture,
448, 365–374.
Zhang, M., Sun, Y., Chen, K., Yu, N., Zhou, Z., Chen, L., … Li, E. (2014).
Characterization of the intestinal microbiota in Pacific white shrimp,
Litopenaeus vannamei, fed diets with different lipid sources. Aquaculture,
434, 449–455.
Zhang, Y., Xie, J., Zhang, Y., & Zhang, M. (2014). Degradation kinetics of ju-
juboside A by rat intestinal flora and identification of the metabolites by
HPLC-­MS/MS. International Journal of Food Properties, 17, 1841–1849.
Zhang, Z., Xu, L., Liu, W., Yang, Y., Du, Z., & Zhou, Z. (2014). Effects of par-
tial replacing soybean meal or cottonseed meal with completely hy-
drolysed feather meal (defatted rice bran as the carrier) on production,
cytokines, adhesive gut bacteria, and disease resistance in hybrid ti-
lapia (Oreochromis niloticus ♀ X Oreochromis aureus ♂). Fish & Shellfish
Immunology, 41, 517–525.
Zheng, Y., Yu, M., Liu, Y., Su, Y., Xu, T., Yu, M., & Zhang, X. (2016). Comparison
of cultivable bacterial communities associated with Pacific white
shrimp (Litopenaeus vannamei) larvae at different health statuses and
growth stages. Aquaculture, 451, 163–169.
|
      665
Zhou, C. P., Lin, H. Z., Ge, X. P., Niu, J., Wang, J., Wang, Y., … Tan, X. H.
(2015). The Effects of dietary soybean isoflavones on growth, innate
immune responses, hepatic antioxidant abilities and disease resis-
tance of juvenile golden pompano Trachinotus ovatus. Fish & Shellfish
Immunology, 43, 158–166.
Zhou, Z., Yao, B., Romero, J., Waines, P., Ringø, E., Emery, M., … Merrifield,
D. L. (2014). Methodological approaches used to assess fish gastroin-
testinal communities. In D. Merrifield, & E. Ringø (Eds.), Aquaculture nu-
trition: Gut health, probiotics and prebiotics (pp. 101–127). Oxford, UK:
Wiley-Blackwell Publishing.
Zwielehner, J., Lassi, C., Hippe, B., Pointer, A., Switzeny, O. J., Remely, M.,
… Haslberger, A. G. (2011). Changes in human fecal microbiota due to
chemotherapy analysed by TaqMan-­PCR, 454 sequencing and PCR-­
DGGE fingerprinting. PLoS ONE, 6, e28654.
How to cite this article: Zhou Z, Ringø E, Olsen RE, Song SK.
Dietary effects of soybean products on gut microbiota and
immunity of aquatic animals: A review. Aquacult Nutr.
2018;24:644–665. https://doi.org/10.1111/anu.12532.