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Current Biochemical Engineering, 2014, 1, 2-8

Recent Advances in Solid-State Fermentation Applications for the Food

Industry
Maria Papagianni*
Department of Hygiene and Technology of Food of Animal Origin, Faculty of Veterinary Medicine, Aristotle University
of Thessaloniki, Thessaloniki 54 124, Greece
Abstract: Solid state fermentation (SSF) has been receiving increased interest during the recent years as an attractive alternative to costly submerged fermentation (SmF) processes for specific applications relative to the food industry. Progress in understanding of biochemical engineering aspects, new bioreactor designs and innovative applications have been
the main forces that have led to the renewed interest for a long-known and mostly neglected fermentation technique. The
present review focuses on the recent advances in SSF applications for the production of metabolites with important applications in the food processing industry, e.g. organic acids, enzymes, flavour compounds and gums.

Keywords: Food industry, metabolites, solid-state fermentation.

1. INTRODUCTION
SSF has been used extensively in the production of fermented foods since ancient times. Soy sauce, vinegar, the
Roquefort cheese and Chinese wine, are only a few examples
of foods that continue to be produced since antiquity through
established SSF processes. Now a days, apart from food production, established SSF processes span from the production
of industrial enzymes [1-5] to value-added fine products,
such as ethanol, single-cell protein, organic acids, amino
acids, secondary metabolites, mushrooms, and others [6-9].
The interest in SSF is significant and keeps increasing according to the large amount of published research that proves
its potential in areas such as biorefineries, bioremediation,
antibiotic production and even fungal spores production [10].
Today, a large number of microbial fermentation products are increasingly utilized as food additives or supplements. The most common among these include substances
that serve as antioxidants, preservatives, flavourings, colorants and sweeteners. Several studies have shown that production in SSF systems may be inferior as a process compared to
SmF because of higher yields, lower costs or even better
product characteristics. These have been most recently reviewed by Singhania et al. [10].
The nature and characteristics of the solid substrate is the
parameter with the greatest influence on process productivities. The solid substrate is the source of nutrients and the
immobilization matrix for the culture. The provided area for
microbial growth and the water activity are critical parameters in any SSF process. Substrate availability and costs underline the SSF process economics. Research in this area is
mainly focused on the selection of suitable substrates among
*Address correspondence to this author at the Department of Hygiene and
Technology of Food of Animal Origin, Faculty of Veterinary Medicine,
Aristotle University of Thessaloniki, Thessaloniki 54 124, Greece; Tel: +30
2310 999804; Fax: +30 2310 999829; E-mail: mp2000@vet.auth.gr
2212-7127/14 $58.00+.00

various agro-industrial residues [10]. Filamentous fungi can

utilize even the hardest of solid substrates offering the advantage of efficient utilization of low-cost substrates and
value addition for wastes [5, 11, 12].
SSF systems require much simpler technology and less
energy requirements compared to the highly sophisticated
SmF systems. However, difficulties in mixing, scaling-up,
and effective control of process parameters like pH, temperature, moisture and others, as well as difficulties in product
recovery, represent serious limitations on SSF applications.
Extensive research in the area of biochemical engineering
aspects of SSF aims to reduce the impact of these problems
[13]. Novel bioreactor designs have been proposed, while
modelling and process optimization studies contribute to the
establishment of more effective design and control criteria of
SSF processes [10, 14, 15].
The aim of the present paper is to give an overview of the
applications -established or potential- of SSF processes for
the production of metabolites of commercial importance to
the food industry. Organic acids (citric and lactic acid), enzymes (
-amylase, invertase, lipases, pectinases, proteases),
flavour compounds and gums production through SSF will
be discussed.
2. SSF APPLICATIONS OF COMMERCIAL IMPORTANCE TO THE FOOD INDUSTRY
2.1. Organic Acids
2.1.1. Lactic Acid
Lactic acid, a commonly occurring organic acid, is an
industrially important product with wide use in the food,
pharmaceuticals and polymers industries. It can be produced
either by chemical synthesis from petrochemical resources or
by microbial fermentation. Currently, almost all lactic acid
produced globally is the product of fermentation processes
[16]. Fermentation offers the advantage of an optically
2014 Bentham Science Publishers

Recent Advances in Solid-state Fermentation Applications for the Food Industry

highly pure product by employing appropriate strains, while

chemical synthesis always results in racemic mixtures of
DL-lactic acid [17]. In addition, fermentation offers the advantage of the utilization of cost effective substrates and
lower temperatures, altogether resulting in more effective
and economical production processes. Batch, fed-batch, repeated batch and continuous submerged fermentations are
the most frequently used methods for lactic acid production.
Although the economics of a fermentation process for lactic
acid production depend on many factors, the cost of raw materials remain the critical one and currently, research is focused on the potential of utilization of various renewable
resources and in particular lignocellulosic materials, as substrates [16-19].
Production of lactic acid through SSF was studied in several cases using lactic acid bacteria (LAB) or fungi and various substrates. LAB are used traditionally in SSF-based food
fermentations and ensiling of various agricultural residues
and therefore are able to grow in SSF systems. Their potential however, as effective producers of lactic acid in SSF
systems was firstly investigated by Xavier and Lonsane in
1994 [20]. In that case, Lactobacillus casei was cultivated in
an SSF system using sugar cane pressmud and produced the
maximum of 5.27 g per 100 g dry sugar cane pressmud,
which was a generally high yield. In the same year, Richter
and Trger [21] reported the L(+)-lactic acid production in
SSF by L. paracasei using sweet sorghum as the solid substrate.
Lactobacillus casei was also used by Rojan et al. [22] for
the production of L(+)-lactic acid in SSF with sugarcane
bagasse as the inner support soaked with cassava starch hydrolysate. The maximum obtained yield corresponded to a
97% conversion of sugar to lactic acid. Lactic acid yield in
that case was 49 g per 100 g starch. Naveena ad co-workers
[23, 24] used L. amylophilus and wheat bran as both support
and substrate.
In a more recent study, Ray and Panda [25] employed
L. plantarum and cassava fibrous residue in a semi-solid
fermentation system supplemented with MRS liquid medium. Most recent works report the production of lactic acid
in SSF with L. plantarum grown on tea wastes [26], and the
use of various Lactobacillus strains (e.g. L. delbrueckii, L.
pentosus) grown on pine needles [27] or wheat bran beds, in
pure cultures or co-cultures [28]. The described systems [2628] showed good compatibility of the bacteria with the solid
substrates employed and lactic acid production approximated
45 g/L.
Fungal Rhizopus sp. have long been recognized as suitable producers of lactic acid that, unlike the LAB, generate
only the L(+) form of the acid [29]. Soccol et al. [30] studied
the production of L(+) lactic acid by R. oryzae in SSF with
sugarcane bagasse as a support and reported a slightly higher
productivity than in submerged cultivation. In a recent study,
R. oryzae was cultivated on cassava pulp and was found to
be able to give the titer of 206.20 mg lactic acid per g initial
dry pulp [31]. Using commercial glucoamylase and cellulose, the titer was increased to the significant 463.18 mg lactic acid per g initial dry pulp.

Current Biochemical Engineering, 2014, Vol. 1, No. 1

2.1.2. Citric Acid

Citric acid, the most important organic acid produced at
industrial level, is also the most commonly used organic acid
in the food industry. It is used as acidifier, flavour enhancer,
antioxidant and antifoam agent. Citric acid is also used extensively by the pharmaceutical and chemical industries.
Although citric acid can be produced by chemical synthesis,
the method is expensive and fermentation has long gained
the preference as the method of industrial production. Currently, citric acid is mainly produced by the filamentous fungus A. niger in SmF [32, 33].
Production of citric acid through SSF is the alternative
commercial method of production. Aspergillus niger is
again the mostly employed microorganism, while a variety
of agro-industrial wastes are used as substrates e.g. sugarcane bagasse, wheat bran, fruit wastes, rice bran, coffee
husk, corncob and others [34]. In recent years, SSF is gaining increased attention for the production of citric acid for
economic reasons because of the low cost of agro-industrial
wastes and the ability of the fungus to grow efficiently on
them while producing significant amounts of acid.
As with the submerged process, production of citric acid in
SSF depends on the employed strain and the process parameters. Aeration is critical and the increased oxygen demand of
the process is met through forced aeration and agitation [35,
36]. The type of the substrate has been extensively studied
since a large variety of agro-industrial wastes have been tested
for their potential use as substrates for citric acid production
[37]. Using inexpensive substrates, such as orange and pineapple waste, apple and grape pomace, kiwifruit peel, rice and
wheat bran, carrot waste, carob pod, cassava bagasse, coffee
husk, and mussel processing wastes [37-43], the costs of the
process can be reduced. To assist the utilization of the raw
material by the fungus, often this is pre-treated and supplemented with nitrogen and phosphorus sources [34, 43]. It has
also been shown that addition of lower alcohols (methanol,
ethanol, isopropanol), methyl acetate, copper, magnesium and
zinc, enhances acid production [44, 45]. In most of this type of
works, optimization studies were performed using central
composite designs or other statistical methods. The reported
yields in many cases exceeded a 70%, based on the consumed
sugars. Pandey et al. [42], using cassava bagasse and A. niger
NRRL 2001, obtained 27 g citric acid per 100 g dry substrate
under optimum fermentation conditions, corresponding to
70% yield. Prado et al. [43], using another strain of A. niger
and thermally pre-treated cassava bagasse obtained a similar
yield. However, Vandenberghe et al. [46] using again cassava
bagasse and an Aspergillus niger strain compared various
types of reactors (flasks, trays, columns and an horizontal
drum fermenter) and reported the highest production of 30.9 g
citric acid per 100 g dry substrate in a column fermenter. The
highest reported yield was 34.24 g citric acid per 100 g dry
substrate by Dhillon and co-workers [47] obtained with A.
niger NNRL 567 cultivated on apple pomace and rice husk in
plastic trays.
2.2. Enzymes
2.2.1.
-Amylases
The term amylase refers to
-, -amylase, and glucoamylase enzymes. Although these can be derived from

4 Current Biochemical Engineering, 2014, Vol. 1, No. 1

plant, animal and microbial sources, the latter represent the

main way of production as they generally meet industrial
demands. Today, a large number of amylases of microbial
origin (fungal and bacterial) are available commercially,
with
-amylases ranking first in terms of commercial exploitation [48].
-Amylases (EC 3.2.1.1) are used commercially
in the production of glucose and sugar syrups while they are
used extensively by the food-processing industry, as well as
the beverage, textiles and detergent industries. Commercial
production of
-amylases is commonly carried out using
bacteria of the genus Bacillus (e.g. B. subtilis, B. stearothermophilus, B. licheniformis and B. amyloliquefaciens) or
fungi of the genus Aspergillus, through submerged fermentation [49, 50]. The potential of SSF systems however, as
means of production of either bacterial or fungal
-amylase
has been shown in many cases.
Among species of the genus Bacillus used, B. subtilis, B.
licheniformis, B. cereus, B. mesentericus, B. vulgatus, B.
polymyxa, B. mycoides, B. coagulans, B. atterimus, B.
megaterium, have all been shown to be effective producers
of thermostable
-amylases in SSF [9, 51-54]. Various substrates were employed, e.g. wheat, corn and rice bran, fruit
stalks, potato peel, cassava bagasse and others. The reported
yields varied and a direct comparison is rather difficult as
they were expressed in different units. Babu and Satyanarayana [51] used B. coagulans and wheat bran and reported a
maximum
-amylase production of 26,350 U per g dried
substrate in an aerated reactor within 48 hours of cultivation.
Fungal
-amylases can be produced effectively in SSF
systems by various fungi. Sugathi et al. [55] cultivated A.
niger BAN3E, a strain isolated from bread, on a variety of
solid substrates and reported specific activities of 311 U/mg
after 6 days of incubation at 37oC. Supplementation of the
solid substrate with ammonium nitrate led to significant increases in yield. In general, nitrogen supplementation enhances
-amylase production by Aspergillus cultivated on
solid substrates, as was shown in the works of Pandey et al.
[56], Anupama and Ravindra [57] and Ross and Guerra [5]
with A. niger, Got et al. [58] with A. fumigatus, and
Sivaramakrishnan et al. [59] with A. oryzae. Balkan and Ertan [60] reported the production of
-amylase in significant
amounts by Penicillium chrysogenum cultivated on agricultural by-products with wheat bran giving the highest titers of
160 U/ml under optimized conditions. The highest
-amylase
activity of 534 U/g was reported by Kunamneni et al. [61],
using the thermophilic fungus Thermomyces lanuginosus and
wheat bran supplemented with soluble starch and peptone.
2.2.2. Lipases
Lipases (triaglycerol acylhydrolases, EC 3.1.1.3) catalyse
both the hydrolysis and the synthesis of esters formed from
glycerol and long-chain fatty acids. Because of their numerous applications either as hydrolases or as synthetases, they
are used widely by the food, pharmaceutical and chemical
industries [62]. Microbial lipases are produced by bacteria,
yeasts and fungi and most studies on lypolytic enzymes production are carried out in SmF systems. In recent years however, high yields of microbial lipases have been reported
using SSF processes and commercial substrates [63-65].

Maria Papagianni

Filamentous fungi are important producers of lipases in

SSF systems [66]. Strains belonging to the genera of Aspergillus, Rhizopus, Penicillium, Geotrichum and Rhizomucor
have been reported to produce significant amounts of lipases
in SSF systems [67-69]. The yeast Candida rugosa has also
been shown to produce high amounts of lipase in SSF in
several cases [70-72], with the lipolytic activity reaching up
to 120,000 AU/g of dry matter [72]. Bacteria of the genus
Bacillus, e.g. B. coagulans, B. subtilis, and B. stearothermophilus [73-75] are lipase producers and amount as high as
148,932 U/g have been reported by using SSF systems [73].
Several cheap agro-industrial wastes are used as solid
substrates and among these, coconut, ground nut and olive
oil cakes, fruit wastes, sugarcane bagasse and various types
of bran supplemented with oils, and most commonly olive
oil. The presence of triglycerides or fatty acids has been reported to induce lipolytic enzyme secretion by a number of
microorganisms [76]. Therefore, the type of substrate in SSF
can be used to enhance production of lipases and substrates
such as several food and agro-industrial wastes rich in fatty
acids, triglycerides and sugars are particularly suitable [63,
77].

2.2.3. Pectinases
Pectinases are a heterogenous group of enzymes involved
in the break down of pectin from a variety of plants. They
are classified according to their substrate specificity (pectin,
pectic acid and oligo-D-galacturonate), the degradation
mechanism (hydrolysis and transelimination) and the type of
cleavage (random and terminal) [78]. Pectinases are used
widely by the food industry to clarify fruit juices, wine and
alcoholic beverages, to improve oil extraction, to increase
the firmness of fruits and in many other applications [78].
Commercial grade preparations of pectinases are produced
from fungi and mainly Aspergillus sp. [79]. Yeasts (Saccharomyces, Kluyveromyces) and bacteria (Bacillus, Streptomyces) also produce pectinases. SmF and SSF processes
have been used widely for pectinases production by different
types of microorganisms and several studies have shown that
higher productivities are obtained by SSF systems [80].
Solis-Pereira et al. [81] studied polygalactorunase (PGase)
production by A. niger CH4 in SmF and SSF and reported an
11-fold higher production in the latter. Similarly, Kapoor and
Kuhad [82] in a comparative study of production of alkaline
PGases from a Bacillus sp., demonstrated a more than 60times higher enzyme titer per gram of dry matter in SSF than
per mL of culture medium in SmF.
Several agricultural and agro-industrial residues have
been used as solid substrates for pectinase production, e.g.
wheat, rice and soy bran, sugarcane and orange bagasse, citrus fruit peels and pomace, cocoa and coffee pulp and husk,
and others [9, 80, 83, 84]. The highest reported pectinase
activities were obtained by A. carbonarius cultivated on
wheat bran, approximating 500 IU per g of dry substrate [85,
86].
Attempts for genetic improvement of producer microorganisms for increased pectinase production using mutagenesis techniques or protoplast fusion have been successful [87,
88]. Kavitha and Umesh-Kumar [86] carried out interspecific
protoplast fusion of A. niger and A. carbonarius to obtain

Recent Advances in Solid-state Fermentation Applications for the Food Industry

hybrids that produced 6-fold higher pectinase activities and

had improved growth compared to the parent strain of A.
carbonarius on SSF with wheat bran as the sole source of
nutrients.
2.2.4. Proteases
Proteases are enzymes that catalyze the hydrolysis of
peptide bonds in proteins and polypeptides. They occur
widely in plants, animals and microorganisms and thousands
of them have been isolated and characterized. Hundreds of
them are used extensively by the industry and they are
mostly microbial proteases. In food processing, proteases are
used by the dairy and the baking industry, the fish and seafood processing industry, in animal and plant protein processing and in yeast hydrolysis. Food-grade proteases are produced efficiently by several species of Aspergillus, Penicillium, Rhizopus and Mucor fungi, while bacteria of the genera
Bacillus, Streptomyces, Streptococcus and Pseudomonas are
also important protease producers [89].


Microbial proteases are produced both in SmF and SSF
systems. Fungal neutral proteases are the most important
component of commercial fungal protease preparations,
which have applications in baking, food processing, and protein modification. Aspergillus oryzae is the main producer
of this type of proteases [90, 91]. A comparative evaluation
of neutral protease production by A. oryzae in SmF and SSF
reported by Sandhia et al. [92], showed 3.5-fold more enzyme production in SSF, clearly demonstrating the superiority of SSF over SmF for the particular organism and enzyme.
Also, proteases from Aspergillus sp. and Mucor sp. were
produced in higher yields in SSF using wheat bran as the
solid media with 50 % more moisture content than in SmF
[42, 93, 94]. Similar observations were made by Soares et al.
[95] for protease production by the bacterium B. subtilis in
SSF. Using soy cake as substrate, enzyme productivity was
45% higher in SSF than in SmF.
2.3. Flavours
Flavouring compounds represent over a quarter of the
global market for food additives and most of them are products of chemical synthesis or plant extraction. Fermentation
can provide an alternative source of flavours since several
microorganisms are able to synthesize aroma compounds.
Microbial cultures are used to produce flavour compounds
either in situ as part of food fermentations or in fermentation
for the production of food additives. Longo and Sanroman
[96] reviewed the microbial-based methodologies for the
production of food aroma compounds and concluded that the
production of relevant aroma compounds for the food processing industry by the use of microbial cultures offers several
advantages over traditional methodologies, while the use of
SSF can give higher yields or better product characteristics
than SmF with lower costs.
SSF applications in food aroma production have been
described for fungi, yeasts and bacteria. Several methylketones such as 2-undecanone, 2-nonanone and 2-heptanone
are produced at commercial scale by SSF from A. niger using coconut fat as substrate with a yield of 40 % [97, 98].
Aspergillus oryzae [99] and R. ozyzae [100, 101] produce
volatile compounds such as acetaldehyde, methylbutanol and

Current Biochemical Engineering, 2014, Vol. 1, No. 1

others, when cultivated in rice koji and agro-industrial substrates, respectively. Ceratocystis fimbriata strains produce
fruity aromas. Bramorski et al. [102] reported the production
of strong fruity aroma by C. fimbriata in solid-state cultures
using cassava bagasse, apple pomace and soybean. Soares et
al. [103] cultivated C. fimbriata on coffee husk and reported
the production of strong pineapple aroma. Neurospora sp.
also produce fruity aromas in SSF of pre-gelatinized rice
[104]. The basidiomycete, Pycnoporus cinnabarinus has
been used for the direct conversion of ferulic acid, enzymatically released from agricultural wastes such as beet pulp and
cereal bran (maize, wheat), to vanillin [105]. A two-step
process has also been described using first A. niger to transform ferulic into vanillic acid, then P. cinnabarinus to obtain
vanillin from vanillic acid [106, 107].
Sugawara et al. [108] studied the formation of HEMF
(4-hydroxy-2 (or 5)-ethyl-5(or 2)-methyl-3 (2H)-furanone)
aroma components by the yeast Zygosaccharomyces rouxii
in miso. Kluyveromyces marxianus produced monoterpene
alcohols and isoamyl acetate responsible from fruity aromas,
in SSF using cassava bagasse or giant palm bran as solid
substrates [109].
Several bacterial species have been found to be suitable
producers of flavour compounds in SSF. Pyrazines, the food
additives with the nutty and roasty flavour, were produced
by B. subtilis cultivated on soybeans [110, 111]. The lactic
acid bacteria Pediococcus pentosaceus and L. acidophilus
produced significant amounts of butter-flavoured compounds
in semi-solid, maize-based, cultures [112].
2.4. Xanthan Gum
Xanthan gum is an extracellular polysaccharide (EPS)
produced by the bacterium Xanthomonas campestris in submerged fermentation using commonly sucrose or glucose as
the carbon source [113]. Xanthan is the most important microbial EPS with several industrial applications in the food,
pharmaceutical, cosmetics and textile industries. Xanthan
production in SSF was first reported by Stredanski and Conti
[114] and Stredanski et al. [115]. Using a variety of agroindustrial solid substrates e.g. apple and grape pomace, spent
malt grains and citrus peel, they obtained comparable yields
with those obtained from SmF processes. Recently,
Vidhyalakshmi et al. [116] reported increased yields of xanthan (2.9 g/50 g solid substrate) in SSF by X. citri using potato peels as the solid substrate. These studies show that xanthan gum can be produced effectively using cheap raw materials; however, its purity varies and may need extra purification steps to obtain a food-grade product.
3. CONCLUDING REMARKS
The cases discussed in this review demonstrate clearly
the potential of SSF as an effective alternative fermentation
method for the production of metabolites with importance to
the food industry. A large variety of agro-industrial residues
and wastes can replace the costly substrates of SmF while
the yields are comparable or even higher in some cases of
products (e.g. enzymes). However, the industrial production
of metabolites by SSF still remains limited to a small number
of them (e.g. organic acids). The reason lies in difficulties in
scale-up of processes because the nature of the solid sub-

6 Current Biochemical Engineering, 2014, Vol. 1, No. 1

strate involves the presence of gradients in most of the important process parameters such as substrates (including
moisture and oxygen), inoculum, pH, and temperature.
Therefore, bioreactor design with the goal of process scaleup is a crucial area in SSF development. Another area often
regarded as the black box in SSF biotechnology is the microbial biochemistry under the particular conditions of SSF
processes. Elucidation of the physiological background will
lead to improved processes and yields and will expand the
areas of SSF applications.

Maria Papagianni
[15]
[16]

[17]
[18]

[19]

CONFLICT OF INTEREST
The authors confirm that this article content has no conflicts of interest.
ACKNOWLEDGEMENTS

[20]

[21]

Declared none.
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