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Bioreactor design for protein enrichment of agricultural residues by solid

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Article  in  Biochemical Engineering Journal · March 2003

DOI: 10.1016/S1369-703X(02)00132-8

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 Biochemical Engineering Journal 13 (2003) 197–203

Bioreactor design for protein enrichment of agricultural

residues by solid state fermentation
Tim Robinson, Poonam Nigam∗
School of Biomedical Sciences, University of Ulster, Coleraine BT52 1SA, Northern Ireland UK
Received 14 November 2001; accepted after revision 24 July 2002

Abstract
This paper reviews bioreactor designs and their use for protein production under solid state fermentation (SSF) conditions using various
agricultural by-products. The advantages and disadvantages of various bioreactors and their potential for scale-up are described. SSF is
proposed as a suitable low-tech strategy for protein enrichment for animal feed by converting a previously low value substance into a more
nutritionally valuable one. The use of various substrates and microorganisms for protein enrichment are also listed.
© 2002 Elsevier Science B.V. All rights reserved.
Keywords: Agricultural residues; Bioconversion; Bioreactors; Protein; Solid state fermentation

1. Introduction Therefore, as a result of the low Aw in SSF bioreac-

Solid state fermentation (SSF) may be characterised by a
fermentation process carried out on a solid medium with a
low moisture content (Aw ), typically 0.40–0.90, which oc-
curs in a non-septic and natural state [1,2]. SSF has been
successfully exploited for food production [3,4], fuel [5,6],
enzymes [7], animal feeds [8,9] and also for dye degradation
[10–12].
Many of the solids used for SSF are unrefined and are
of agricultural origin [13,14] making complete characterisa-
tion and exact reproducibility difficult [15]. In recent years,
SSF has received more and more interest from researchers,
as studies have demonstrated superior product yields and
simplified downstream processing [16,17]. The use of solid
matter, either as an inert support or substrate/support has,
however, had serious implications on the engineering aspect
of bioreactor design and operation.
The low moisture content means that fermentation can
only be carried out by a limited number of microorganisms,
mainly yeasts and fungi, although some bacteria have been
used [18,19]. This means that although SSF is a non-septic
fermentation, spoilage or contamination by unwanted bacte-
ria is reduced by the low Aw (<0.95), inhibits most bacterial
growth [20–22].
∗ Corresponding author. Tel.: +44-28-7032-4053;
fax: +44-28-7032-4906.
E-mail address: p.nigam@ulst.ac.uk (P. Nigam).
tors, smaller fermenters are required and a more concen-
trated product is produced, simultaneously reducing energy
requirements for downstream processing [23]. Sterilisation
costs are lower due to the limitation of free water, which in
turn reduces operating costs needed for effluent treatment
[2,15].
A large amount of metabolic heat is generated during
SSF and its rate is directly proportional to the level of
metabolic activity in the system [24,25]. Heat transfer in
SSF reactors is not as efficient in comparison to submerged
(liquid) fermentations (SmF). This is mainly due to the
solidness of the substrate and the lack of free water available
during fermentation [15,26]. In laboratory scale reactors,
heat may be removed by keeping the culture vessel in a
temperature-controlled environment, such as a water bath
[27]. Problems in SSF occur when scale-up is considered;
the problem of the lack of free water and generation of
metabolic heat is greatly exaggerated as the system strug-
gles to provide adequate agitation, aeration and cooling.
Temperatures have been reported to be as high as 47–50 ◦ C
on the centre of the fermenting mass by Rathbun and Shuler
[28] and temperatures as high as 60–70 ◦ C by Hayes [29]
in the innermost region.
The use of SSF for protein enrichment of lignocellu-
lose residues has received close attention due its low level
technology, reduced reactor volume per unit weight of sub-
strate converted and its direct applicability of the fermented
product for feeding purposes [30]. Large quantities of fi-
brous crop residues are currently under utilised as potential

1369-703X/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved.
PII: S 1 3 6 9 - 7 0 3 X ( 0 2 ) 0 0 1 3 2 - 8
198 T. Robinson, P. Nigam / Biochemical Engineering Journal 13 (2003) 197–203
animal feed sources, especially in developing countries. A
major reason for this is the low protein content of the waste
residues, which can be enriched utilising added urea as ni-
trogen source through fermentation by white-rot fungi, for
example, as demonstrated by Zadrazil [31].
Three general reactor groups exist for SSF, and each in
their own design, try to make conditions more favourable
for fermentation. This paper will examine from the sim-
ple to the more complex in design for protein enrichment
in order to discover how and why changes have been
made in an attempt to control the major limiting factors in
SSF.
2. Bioreactors for SSF
Three basic groups of reactor exist for SSF, and these
may be distinguished by type of mixing and aeration used.
In laboratory scale, SSF occurs mainly in flasks and the
following reactors used for larger scale product formation.
2.1. Tray bioreactors
Tray bioreactors tend to be very simple in design, with
no forced aeration or mixing for the solid substrate (Fig. 1).
Such reactors are restrictive in the amount of substrate that
can be fermented, as only thin layers can be used, in order
to avoid overheating and to maintain aerobic conditions
[32]. The undersides of the trays are perforated to allow
Fig. 1. A Koji-type tray bioreactor.
aeration of the solid substrate, with each tray arranged
above each other. Temperature and relative humidity are
the only controllable external parameters [14]. Wooden
trays were initially used for soy sauce production in Koji
fermentations by Aspergillus oryzae [33]. The use of tray
reactors has remained largely unchanged, with the only en-
gineering advance being the use of more modern materials
such as, plastic and aluminium. This has been successfully
used for lignocellulose fermentation [33]. The advantage of
plastic or aluminium trays over wooden trays would make
sterilization and cleaning easier and therefore reduce the
possibility of contamination or spoilage.
The use of tray fermenters in large-scale production is
limited as they require a large operational area and tend
to be labour intensive with mechanical handling also being
difficult. It can be seen that the lack of adaptability of this
type of fermenter makes it an unattractive design for any
large-scale production [33].
2.2. Drum bioreactors
Drum bioreactors are designed to allow adequate aeration
and mixing of the solid, whilst limiting the damage to the
inoculum or product (sheer forces or heat build-up). Mixing
and aeration of the medium has been explored in two ways:
by rotating the entire vessel [34,35] or by various agitation
devices, such as paddles and baffles [36,37].
Rotation or the use of agitation can be carried out on
a continuous or periodic basis (Fig. 2), promoting surface
 T. Robinson, P. Nigam / Biochemical Engineering Journal 13 (2003) 197–203 199

Fig. 2. A rotating drum bioreactor.

mass heat transfer and a more uniform distribution of nu-
trients [27]. Growth of the inoculum in drum bioreactors
is considered to be better and more uniform than that in
tray fermenters [33]. Fungal cultures are prone to damage in
both rotating drum bioreactors (RDBs) and mixed reactors,
as the increased sheer forces through mixing, affecting the
ultimate product yield being compromised [33].
Air may be supplied into the vessel via an inlet, with
excess gas escaping through an outlet valve. Temperature
control in drum bioreactors is quite difficult with mixing
along with the growth of the microorganism producing
high temperatures [36]. Any rise in temperature above the
optimal range may have a detrimental effect on product
formation.
Although the mass heat transfer, aeration and mixing of
the substrate is increased, in drum reactors, damage to in-
oculum and heat build-up through sheer forces may af-
fect the final product yield. Application of drum reactors
for large-scale fermentations also poses handling difficulties
[33].
Forced aeration is generally applied at the bottom of the
column, with the humidity of the air kept high to avoid des-
iccation of the substrate. Columns, at lab-scale, are typically
30 cm in height and may be places in water baths in order
to maintain a constant fermentation temperature [38,39]. In
larger-scale fermentations the column temperature can be
controlled by the use of a water jacket [14,15,33]. The use
of thin columns have been reported as helping to facilitate
heat transfer in the solid mass due to the increase in surface
area and therefore avoiding the need for any cooling devices
[15].
Disadvantages associated with packed bed column biore-
actors for SSF include difficulties in obtaining the product,
non-uniform growth, poor heat removal and scale-up prob-
lems [15,40].

2.3. Packed bed bioreactors

Packed bed reactors, usually in the form of a column,

have emerged over the past 20 years as a potential alternative
to the previously mentioned reactors (Fig. 3). Columns are
usually constructed from glass or plastic with the solid sub-
strate supported on a perforated base through which forced
aeration is applied [15]. Packed bed column bioreactors have
been reported to be useful for product developments with ef-
ficient process controls, particularly for heat removal. They
have been used for the production of enzymes, organic acids
and secondary metabolites [23,33]. Fig. 3. A packed column bioreactor.
200 T. Robinson, P. Nigam / Biochemical Engineering Journal 13 (2003) 197–203
3. Current SSF strategies
Many of the current research papers concerning SSF have
tended to focus on reporting lab-scale findings. This is un-
derstandable, as parameters tend to be more controllable,
with data collection simplified and running costs low. There
are therefore few papers describing current state of the art
reactors, giving design and yield details, as this is industri-
ally sensitive material.
Fermentation strategies have scaled-up and adopted to suit
various situations and needs. Singh and Gupta [41], describe
the SSF of cereal straw under a polythene cover, known
as the “Karnal process”. This method is carried out in two
stages, and uses thinly layered substrate as in a tray fer-
menter, but without the use of a perforated tray support. In
the first stage, the cereal straw is treated with 4% urea at a
40% moisture level and is ensiled under the polythene cover
for 30 days. The second stage involves the use of a rectan-
gular brick structure (200 cm × 150 cm) which acts as the
bioreactor. The loosely stacked bricks help provide aeration
from all sides, with a thin layer of urea-treated straw spread
thinly inside the brick enclosure as a nitrogen source for
the fungi. Coprinus fimetarius was added and its subsequent
growth enriched the protein content of the straw. Although
external parameters could not be finely controlled, the brick
reactor and the covering of polythene helped to maintain an
adequate balance between heat generation and loss, and also
allow a reasonable level of aeration.
Tripathi and Yadav [42], also employed a similar strat-
egy to ferment wheat straw using polypropylene bags inoc-
ulated with Pleurotus ostreatus. Their method employed the
use of perforated bags to allow aeration and cooling whilst
ultimately enriching the wheat straw for animal feed.
3.1. Parameter controls in drum reactors
3.1.1. Mixed reactors
A major problem with scale-up is the removal of heat
generated by metabolic activity of the microorganism [43].
Heat removal is limited in a solid mass, with a lack of heat
exchange surface on a large-scale. Current strategies have
concentrated on improving cooling through evaporation of
moisture from the substrate, subsequently reducing the re-
actor temperature. This has however has its disadvantages
with great loss of water [44] and so research has focused on
maintaining a balance between temperature and moisture.
Evaporative cooling may be combined with spraying of wa-
ter onto the substrate to prevent drying [45]. This evapora-
tion and moisture replenishment needs to occur in uniform
over the substrate and mixed bioreactors are required.
Nagel et al. [36], attempted to ensure uniform mixing
of the solid mass allowing adequate and uniform mixing
of the substrate whilst simultaneously maintaining uniform
evaporation and moisture replenishment. This was carried
out in a 35 l bioreactor with a paddle mixer. Six V-shaped
paddles were mounted along a central axis, equidistant and
at 90◦ to each other. This achieved both radial and axial
mixing. Axial mixing was important for homogenous water
distribution in the bed as individual spraying nozzles cannot
spray evenly over the total surface of the bed. Adequate
radial mixing was achieved after six revolutions.
Various studies have also demonstrated that the monitor-
ing of moisture content of the solid substrate is a vital and
necessary aspect of SSF [36,38,46]. Moisture in the SSF
system is required for cooling, as mentioned previously, and
also for the incorporation of water into new microbial cells
[37]. This theory is supported by Oriol et al. [38], who found
that fungal growth could be hampered by limited water avail-
ability.
Nagel et al. [37] estimated that the amount of water
needed for growth of new cells and evaporative cooling was
a moisture content of ∼45%. A model was developed which
allowed the overall water content as well as the extracel-
lular water content to be incorporated in an on-line control
system. Experiments in a 1.5 and 35 l mixed reactor were
carried out to validate the model that was able to predict
experimental moisture control levels to high degree.
3.1.2. Rotating drum bioreactors
Heat removal and mixing in RDBs are carried out through
the rotation of the vessel. The speed of rotation, however,
causes sheer forces to act on the microorganism affect-
ing growth and product formation. The effect of rotational
speed on SSF performance has received much attention
with some studies reporting reduced SSF productivity with
a high rpm [34,47,48]. Other studies by Lindenfelser and
Ciegler [49], indicated that high rotational speeds actually
favoured SSF, possibly due to better aeration and substrate
mixing.
RDBs are designed to aid aeration and heat removal
through the rotational movement of the vessel. This im-
proved mixing and aeration leads to an increase in micro-
bial growth and a subsequent increase in metabolic heat.
Stuart et al. [35] showed that in a 18.7 l reactor, at 50 rpm,
40% less protein was produced in comparison to static ex-
periments. Poor fungal growth due to sheer forces was a
possible explanation for the decline in protein production.
Fermentation on wheat bran at 5 rpm improved heat transfer
by making the substrate more homogenous in temperature,
increasing the surface area and also increasing evaporative
cooling. For any process using RDBs rotational speed, the
loading of solids and aeration characteristics have to be
taken into account.
4. Substrates for protein enrichment by SSF
As previously mentioned crop residues represent a po-
tential source of dietary energy to ruminants if the protein
content of can be enriched. As these residues are renew-
able and in an abundant supply (∼3.5 billion tonnes of
agricultural by-products per year) they represent a potential
 T. Robinson, P. Nigam / Biochemical Engineering Journal 13 (2003) 197–203
Table 1
Various substrates and microorganisms used for protein enrichment of agricultural waste residues (some examples)
Substrate Microorganism
Apple pomace C. utilis, Kloeckera apiculata, Saccharomyces cerevisae, C. utilis, C. tropicalis,
Trichoderma viriae, A. niger
Canola meal Aspergillus carbonarius
Carob pods A. niger
Grape stalks, orange peels Agrocybe aegirata, Amillarialla mellea, P. ostreatus
Sugarcane baggase Chaetomium celluloticum
solution to feeding animals in developing countries [33].
Table 1 shows a selection of substrates and microorgan-
isms used for the protein enrichment of agricultural waste
residues.
4.1. SSF of starchy material
Cassava is an important food for millions of people in
Africa, Asia and South America. It is, however, low in pro-
tein, vitamins and minerals, as well as sulphur containing
amino acids [19,33]. Sterz et al. [56] found that Rhizopus
formusa was a suitable fungus for improving the nutritional
quality of raw cassava flour. Other studies by Soccol et al.
[57] looked at the biotransformation of cassava [57,58] and
cassava wastes [42,59–61] for nutritional improvement, us-
ing various strains of Rhizopus sp. Raimbault and Germon
[62] increased protein enrichment of cassava to the extent of
20%. This was achieved in a 30 h fermentation period with
Aspergillus niger. Other microorganisms used for cassava
enrichment include R. olegosporus and A. oryzae [63]. Re-
search has also been carried out in a farm setting [64] and
on a pilot plant scale [65].
4.2. SSF of lignocellulosic material
Lignocellulosic crop residues may be characterised by
being high in cellulose, hemicellulose and lignin, but low
in protein. They tend to be difficult to digest by ruminants
and so are limited as potential animal feed [19,33]. The
SSF of these residues has been explored using fungi for
protein enrichment [30,31,66–68]. The use of temperate
lignocellulosic wastes, such as wheat straw, has been exam-
ined by many researchers [41,42,69]. The use of rice and
maize straw in developing countries may also be exploited
[33,41].
4.3. SSF of citrus wastes
Citrus wastes are wastes remaining after juicing on an
industrial scale. These dried peels contain simple sugars,
pectin and cellulose but are low in protein [30,70,71]. A.
niger has been reported to utilise the dried citrus peels un-
der SSF conditions, by fermenting the simple sugars present
[30].
201
Reference
[50,51]
[52]
[53]
[54]
[55]
4.4. SSF of apple pomace
After pulping, apple pomace, which consists of crushed
skins, pips and stalks may be fermented for protein enrich-
ment. It has a high sugar content, as well as a high mois-
ture content (∼80%) which poses disposal problems for the
pulping industry. Unfermented apple pomace had been pre-
viously fed directly to pigs, but was mostly dumped in land-
fill sites [30]. The use of co-cultures of yeasts and fungi to
enrich the protein content of the pomace has been explored
by Bhalla and Joshi [72]. Protein and pectin increased by 20
and 17%, respectively, when apple pomace was fermented
by Candida utilis and A. niger under SSF conditions.
4.5. SSF of carob pobs
Carob or locust tree (Ceratunia siliqua) is found exten-
sively in Mediterranean countries, with the pods containing
large amounts of sugars, making them an attractive substrate
for protein enrichment by SSF. Carob pods also contain high
amounts of tannin, which has an adverse effect on animal
growth [30]. Tannins may be degraded by certain fungi, in-
cluding A. niger [72] whilst also being simultaneously en-
riching the protein content of the carob pods [73]. Protein
enrichment of 20% was achieved in 4 days of SSF with a
83% tannin decrease by Smail et al. [53].
5. Conclusions
The potential advantages of SSF for protein enrichment
can be seen if scale-up parameters, such as cooling and
heat transfer can be more easily controlled. The low Aw , al-
though benefiting the inoculum in terms of competition, has
a detrimental effect on the basis of heat transfer. Metabolic
heat generated by rapidly growing microorganisms due to
better mixing and aeration of reactors, also poses problems
for the SSF system affecting product formation. Additional
heat through the friction of mixing supplements to the
problems of heat exchange. SSF can produce a more con-
centrated protein product that may be used as an animal
feed in both developing and developed countries. As SSF
bioreactors have increased in size in order to try and in-
crease the product concentration so too have the problems
202 T. Robinson, P. Nigam / Biochemical Engineering Journal 13 (2003) 197–203
concerning parameter controls. The benefits of SSF for
protein enrichment maybe better realised in situ, on farms
in developing countries, which can avail of this relatively
low-tech fermentation system. It is apparent that SSF may
be a viable technology for the enrichment of previously
worthless waste residues for animal feed.
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