Application of solid-state fermentation to food industry-A review

Application of solid-state fermentation to food industry-A review
Journal of Food Engineering 76 (2006) 291–302

 Application of solid-state fermentation to food industry—A review
                               Susana Rodrı́guez Couto                      , Ma Ángeles Sanromán                a,*

                  Department of Chemical Engineering, Isaac Newton Building, University of Vigo, Lagoas Marcosende, 36310 Vigo, Spain
                  Department of Chemical Engineering, Chemical Engineering School, Rovira i Virgili University, 43007 Tarragona, Spain

                                                  Received 9 November 2004; accepted 19 May 2005
                                                            Available online 20 July 2005


    Solid state fermentation (SSF) has become a very attractive alternative to submerged fermentation (SmF) for specific applications
due to the recent improvements in reactor designs. This paper reviews the application of SSF to the production of several metabo-
lites relevant for the food processing industry, centred on flavours, enzymes (a-amylase, fructosyl transferase, lipase, pectinase),
organic acids (lactic acid, citric acid) and xanthan gum. In addition, different types of biorreactor for SSF processes have been
Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: Bioreactors; Enzyme production; Food processing industry; Solid-state fermentation

1. Introduction                                                               liquid (Pandey, 1992). The low moisture content means
                                                                              that fermentation can only be carried out by a limited
    Microorganisms have long played a major role in the                       number of microorganisms, mainly yeasts and fungi,
production of food (dairy, fish and meat products) and                         although some bacteria have also been used (Pandey,
alcoholic beverages. In addition, several products of                         Soccol, & Mitchell, 2000a). Some examples of SSF pro-
microbial fermentation are also incorporated into food                        cesses for each category of microorganisms are reported
as additives and supplements (antioxidants, flavours,                          in Table 1.
colourants, preservatives, sweeteners, . . .). There is great                    SSF offers numerous advantages for the production
interest in the development and use of natural food and                       of bulk chemicals and enzymes (Hesseltine, 1977;
additives derived from microorganisms, since they are                         Pandey, Selvakumar, Soccol, & Nigam, 1999a; Soccol,
more desirable than the synthetic ones produced by                            Iloki, Marin, & Raimbault, 1994). This process is known
chemical processes.                                                           from ancient times and different fungi have been culti-
    Solid-state fermentation (SSF) reproduces the natural                     vated in SSF for the production of food. Typical exam-
microbiological processes like composting and ensiling.                       ples of it are the fermentation of rice by Aspergillus
In industrial applications this natural process can be uti-                   oryzae to initiate the koji process and Penicillium roque-
lised in a controlled way to produce a desired product.                       fortii for cheese production. Also, in China, SSF has
    SSF is defined as any fermentation process performed                       been used extensively to produce brewed foods (such as
on a non-soluble material that acts both as physical sup-                     Chinese wine, soy sauce and vinegar) since ancient time
port and source of nutrients in absence of free flowing                        (Chen, 1992). Also, in Japan SSF is used commercially
                                                                              to produce industrial enzymes (Suryanarayan, 2003).
                                                                              Since 1986 in Brazil a series of research projects for the
     Corresponding author. Tel.: +34 986 812383; fax: +34 986 812380.         value-addition of tropical agricultural products and
     E-mail address: (Ma. Á. Sanromán).                   sub-products by SSF has been developed due to the high

0260-8774/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
292                                                   Sanromán / Journal of Food Engineering 76 (2006) 291–302
                                     S.R. Couto, Ma. A.

Table 1                                                                      & Nigam, 2003). Castilho, Alves, and Medronho (2000),
Main groups of microorganisms involved in SSF processes (extracted           have performed a detail economic analysis of the pro-
from Raimbault, 1998)
                                                                             duction of Penicillium restrictum lipase in both SmF
Microflora                             SSF process                            and SSF. They found that for a production scale of
Bacteria                                                                     100 m3 lipase concentrate per year, total capital invest-
  Bacillus sp.                        Composting, natto, amylase             ment needed for SmF was 78% higher than that needed
  Pseudomonas sp.                     Composting
  Serratia sp.                        Composting
                                                                             for SSF. Also, SSF unitary product cost was 47% lower
  Streptococcus sp.                   Composting                             than the selling price. These studies pointed out that the
  Lactobacillus sp.                   Ensiling, food                         great advantage of SSF processes is the extremely cheap
  Clostridium sp.                     Ensiling, food                         raw material used as main substrate. Therefore, SSF is
Yeast                                                                        certainly a good way of utilising nutrient rich solid
  Endomicopsis burtonii               Tape cassava, rice                     wastes as a substrate. Both food and agricultural wastes
  Saccharomyces cerevisiae            Food, ethanol                          are produced in huge amounts and since they are rich in
  Schwanniomyces castelli             Ethanol, amylase
                                                                             carbohydrates and other nutrients, they can serve as a
Fungi                                                                        substrate for the production of bulk chemicals and en-
  Altemaria sp.                       Composting                             zymes using SSF technique.
  Aspergillus sp.                     Composting, industrial, food
                                                                                The nature of the solid substrate employed is the
  Fusarium sp.                        Composting, gibberellins
  Monilia sp.                         Composting                             most important factor affecting SSF processes and its
  Mucor sp.                           Composting, food, enzyme               selection depends upon several factors mainly related
  Rhizopus sp.                        Composting, food, enzymes,             with cost and availability and, thus, may involve the
                                      organic acids                          screening of several agro-industrial residues. In SSF pro-
  Phanerochaete chrysosporium         Composting, lignin degradation
                                                                             cess the solid substrate not only supplies the nutrients to
  Trichoderma sp.                     Composting, biological control,
                                      bioinsecticide                         the culture but also serves as an anchorage for the
  Beauveria sp., Metharizium sp.      Biological control, bioinsecticide     microbial cells. Among the several factors, which are
  Amylomyces rouxii                   Tape cassava, rice                     important for microbial growth and activity in a partic-
  Aspergillus oryzae                  Koji, food, citric acid                ular substrate, particle size and moisture level/water
  Rhizopus oligosporus                Tempeh, soybean, amylase, lipase
                                                                             activity are the most critical (Auria, Palacios, & Revah,
  Aspergillus niger                   Feed, proteins, amylase,
                                      citric acid                            1992; Barrios-Gonzalez, Gonzalez, & Mejia, 1993;
  Pleurotus oestreatus, sajor-caju    Mushroom                               Echevarria, Leon, Espinosa, & Delgado, 1991; Liu
  Lentinus edodes                     Shii-take mushroom                     & Tzeng, 1999; Pandey, Ashakumary, Selvakumar, &
  Penicilium notatum, roquefortii     Penicillin, cheese                     Vijayalakshmi, 1994; Pastrana, Gonzalez, Pintado, &
                                                                             Murado, 1995; Roussos, Raimbault, Prebois, & Lon-
                                                                             sane, 1993; Sarrette, Nout, Gervais, & Rombouts, 1992;
amounts of agricultural residues generated by this coun-                     Smail, Salhi, & Knapp, 1995; Zadrazil & Punia, 1995).
try (Soccol & Vandenberghe, 2003). Thus, the produc-                            Generally, smaller substrate particles provide a larger
tion of bulk chemicals and value-added fine products                          surface area for microbial attack but if they are too
such as ethanol, single-cell protein (SPC), mushrooms,                       small may result in substrate agglomeration as well as
enzymes, organic acids, amino acids, biologically active                     poor growth. In contrast, larger particles provide better
secondary metabolites, etc. (Hölker, Höfer, & Lenz,                        aeration but a limited surface for microbial attack.
2004; Pandey, 1992; Pandey, 1994; Pandey, Azmi,                              Therefore, a compromised particle size must be selected
Singh, & Banerjee, 1999b; Pandey et al., 1999c; Pandey,                      for each particular process (Pandey et al., 1999a).
Nigam, & Vogel, 1988; Pandey et al., 2000b; Pandey                              Research on the selection of suitable substrates for
et al., 1999d; Vandenberghe, Soccol, Pandey, & Lebea-                        SSF has mainly been centred around agro-industrial resi-
ult, 2000) has been produced from these raw materials                        dues due to their potential advantages for filamentous
by means of SSF technique.                                                   fungi, which are capable of penetrating into the hardest
   In recent years, SSF has received more and more                           of these solid substrates, aided by the presence of turgor
interest from researchers, since several studies for en-                     pressure at the tip of the mycelium (Ramachandran
zymes (Pandey et al., 1999a), flavours (Ferron, Bonna-                        et al., 2004). In addition, the utilisation of these agro-
rame, & Durand, 1996), colourants (Johns & Stuart,                           industrial wastes, on the one hand, provides alternative
1991) and other substances of interest to the food indus-                    substrates and, on the other, helps in solving pollution
try have shown that SSF can give higher yields                               problems, which otherwise may cause their disposal
(Tsuchiya et al., 1994) or better product characteristics                    (Pandey et al., 1999a).
(Acuña-Arguelles, Gutierrez-Rojas, Viniegra-González,                         SSF offers numerous advantages over SmF such as
& Favela-Torres, 1995) than submerged fermentation                           simpler technique and lower cost (Table 2). However,
(SmF). In addition, costs are much lower due to the effi-                      there are few designs available in the literature for biore-
cient utilisation and value-addition of wastes (Robinson                     actors operating in solid-state conditions. This is princi-
 Sanromán / Journal of Food Engineering 76 (2006) 291–302
                              S.R. Couto, Ma. A.                                                                            293

Table 2                                                                  Several researchers have studied the production of ar-
Advantages and disadvantages of SSF over SmF                          oma compounds by SSF from several microorganisms
Advantages                    Disadvantages                           such as Neurospora sp. (Pastore, Park, & Min, 1994),
Higher productivity           Difficulties on scale-up                  Zygosaccharomyces rouxii (Sugawara, Hashimoto,
Better oxygen circulation     Low mix effectively                      Sakurai, & Kobayashi, 1994), Aspergillus sp. (Ito,
Low-cost media                Difficult control of process              Yoshida, Ishikawa, & Kobayashi, 1990), using pre-
                              parameters (pH, heat, moisture,
                              nutrient conditions, . . .)
                                                                      gelatinised rice, miso and cellulose fibres, respectively.
Less effort in downstream      Problems with heat build-up             Bramorski, Soccol, Christen, and Revah (1998) com-
   processing                                                         pared fruity aroma production by Ceratocystis fimbriata
Reduced energy and cost       Higher impurity product, increasing     in solid-state cultures using several agro-industrial
   requirements               recovery product costs                  wastes (cassava bagasse, apple pomace, amaranth and
Simple technology
Scarce operational problems
                                                                      soybean), determining that the media with cassava ba-
It resembles the natural                                              gasse, apple pomace or soybean produced a strong fru-
   habitat for several                                                ity aroma. Soares, Christen, Pandey, and Soccol (2000)
   microrganisms                                                      also reported the production of strong pineapple aroma
                                                                      when SSF was carried out using coffee husk as a sub-
                                                                      strate by this strain. Bramorski, Christen, Ramirez, Soc-
pally due to several problems encountered in the control              col, and Revah (1998) and Christen, Bramorski, Revah,
of different parameters such as pH, temperature, aera-                 and Soccol (2000) described the production of volatile
tion and oxygen transfer and moisture. SSF lacks the                  compounds such as acetaldehyde and 3-methylbutanol
sophisticated control mechanisms that are usually asso-               by the edible fungus Rhizopus oryzae during SSF on
ciated with SmF. Control of the environment within the                tropical agro-industrial substrates.
bioreactors is also difficult to achieve, particularly tem-                Kluyveromyces marxianus produced aroma com-
perature and moisture.                                                pounds, such as monoterpene alcohols and isoamyl ace-
   The aim of this paper is to review the potential appli-            tate (responsible for fruity aromas), in SSF using
cation of SSF for the production of several metabolites               cassava bagasse or giant palm bran as a substrate
of great interest to the food industry. In addition, differ-           (Medeiros et al., 2001).
ent types of biorreactor for SSF processes are described.                Esters are the source of the aromas and among them
                                                                      pyrazines, which possess a nutty and roasty flavour, are
                                                                      used as a food additive for flavouring (Seitz, 1994). Bes-
2. Some examples of applications of SSF to food industry              son, Creuly, Gros, and Larroche (1997) and Larroche,
                                                                      Besson, and Gros (1999) studied the production of
2.1. Flavours                                                         2,5-dimethylpyrazine (2,5-DMP) and tetramethyl-
                                                                      prazine (TTMP) using B. natto and B. subtilis, respec-
   Flavours comprise over a quarter of the world mar-                 tively, on soybeans in SSF. They found that SSF
ket for food additives. Most of the flavouring com-                    was very suitable for the production of these
pounds are produced via chemical synthesis or by                      compounds.
extraction from natural materials. However, recent mar-
ket surveys have shown that consumers prefer foodstuff
                                                                      2.2. Enzyme production
that can be labelled as natural. Plants have been major
sources of essential oils and flavours but their use de-
                                                                         Recently, dos Santos, Souza da Rosa, DalÕBoit,
pends on natural factors difficult to control such as
                                                                      Mitchell, and Krieger (2004) evaluated whether SSF is
weather conditions and plant diseases. An alternative
                                                                      the best system for producing enzymes. They found that
route for flavour synthesis is based on microbial biosyn-
                                                                      SSF is appropriate for the production of enzymes and
thesis or bioconversion (Janssens, de Pooter, Van-
                                                                      other thermolabile products, especially when higher
damme, & Schamp, 1992). Several microorganisms,
                                                                      yields can be obtained than in SmF.
including bacteria and fungi, are currently known for
their ability to synthesise different aroma compounds.
Attempts to use these microorganisms in SmF resulted                  2.2.1. a-Amylase
in low productivity of aroma compounds (Yamguchi                         a-Amylases (endo-1,4-a-D-glucan glucanohydrolase
et al., 1993), which hampered their industrial applica-               EC are extra-cellular endo enzymes that ran-
tion. SSF could be of high potential for this purpose                 domly cleave the 1,4-a linkages between adjacent glu-
(Berger, 1995). Thus, Ferron et al. (1996) reviewed the               cose units in the linear amylose chain and ultimately
prospects of microbial production of food flavours                     generates glucose, maltose and maltotriose units. Since
and the recommended SSF processes for their                           the 1950s, fungal amylases have been used to manufac-
production.                                                           ture sugar syrups containing specific mixtures of sugars
294                                          Sanromán / Journal of Food Engineering 76 (2006) 291–302
                            S.R. Couto, Ma. A.

that could not be produced by conventional acid hydro-              2.2.2. Fructosyl transferase
lysis of starch. Amylases are extensively employed in                  Fructosyl transferase (EC catalyses the
processed-food industry such as baking, brewing, prepa-             formation of fructo-oligosaccharides from sucrose.
ration of digestive aids, production of cakes, fruit juices,        Fructo-oligosaccharides are present in various com-
starch syrups, etc.                                                 monly consumed foods like fruits, vegetables, cereals
   The production of a-amylases has generally been car-             and honey in trace amounts. The production of fructosyl
ried out using SmF; however, SSF systems appear as a                transferase derived from microorganisms has attracted
promising technology. Recently, Francis et al. (2003)               attention in recent years by SmF using Aspergillus spp,
used spent brewing grains in SSF for the production                 Penicillium spp and Aureobasidium spp (Prapulla, Sub-
of a-amylase and determined that the supplement of fer-             haprada, & Karanth, 2000) and SSF using both Aspergil-
mentation media with Tween-80 or calcium ions en-                   lus foetidus and A. oryzae (Hang, Woodams, & Jang,
hanced a-amylase activity.                                          1995; Sangeetha, Ramesh, & Prapulla, 2004).
   Krishna and Chandrasekaran (1996) used banana                       Recently, Sangeetha et al. (2004) have studied the
fruit stalk as a substrate in SSF with Bacillus subtilis.           production of fructosyl transferase by A. oryzae employ-
Different factors such as initial moisture content, parti-           ing a great variety of agricultural by-products as sub-
cle size, thermal treatment time and temperature, pH,               strates: Cereal brans (wheat bran, rice bran and oat
incubation temperature, additional nutrients, inoculum              bran), corn products (corn cob, corn bran, corn germ,
size and incubation period on the production of a-amy-              corn meal, corn grits and whole corn powder), coffee-
lase were characterised. Results obtained for the optimi-           and tea-processing by-products (coffee husk, coffee pulp,
sation of process parameters clearly shown their impact             spent coffee and spent tea), sugarcane bagasse and cas-
on the gross yield of enzymes as well as their indepen-             sava bagasse. They found that, among them, the best re-
dent nature in influencing the organismÕs ability to syn-            sults were obtained when rice bran, wheat bran, corn
thesise the enzyme. It is known that particle size (specific         germ, spent coffee and tea were used supplemented with
surface area) is a critical factor in SSF. Banana fruit             yeast extract and complete synthetic media.
stalk particles of 400 lm favoured maximal a-amylase
production compared to larger particles. A similar                  2.2.3. Lipase
trend was reported for the production of glucoamylases                  Lipases (triacylglycerol acylhydrolases, EC
with wheat bran (Pandey, 1991) and cellulases with coir             are well known as efficient biocatalysts for the hydroly-
pith of small particle size (Muniswaran & Charyulu,                 sis of water-insoluble fatty-acid esters, being triacylgly-
1994).                                                              cerols of long chain fatty acids their natural substrates.
   Nowadays, gelatinisation is coupled with liquefac-               Lipases are nowadays widely used at industrial scale
tion, which is possible by the action of thermostable               with applications in food, detergent, cosmetic and phar-
amylases, which have been reported in both SmF (Stam-               maceutical industries (Jaeger & Reetz, 1998).
ford, Stamford, Coelho, & Araujo, 2001) and SSF                         Most studies on lipolytic enzymes production by bac-
(Babu & Satyanarayana, 1995). Sodhi, Sharma, Gupta,                 teria, fungi and yeasts have been performed in sub-
and Soni (2005) determined that the productivity of                 merged cultures; however, there are few reports on
thermostable amylases from Bacillus sp. was affected                 lipase synthesis in solid state cultures. In recent years,
by the nature of the solid substrate (wheat bran, rice              increasing attention has been paid to the conversion of
bran, corn bran and combination of two brans), nature               processing industry wastes in lipase by solid state
of the moistening agent, level of moisture content,                 cultures.
incubation temperature, presence or absence of sur-                     There are several reports dealing with extracellular li-
factant, carbon, nitrogen, mineral, amino acid and                  pase production by fungus such as Rizhopus sp., Asper-
vitamin supplements. Maximum enzyme production                      gillus sp., Penicillium sp. on different solid substrates
was obtained on wheat bran supplemented with glycerol               (Christen, Angeles, Corzo, Farres, & Revah, 1995; Cor-
(1.0%, w/w), soyabean meal (1.0%, w/w), L-proline                   dova et al., 1998; Gombert, Pinto, Castilho, & Freire,
(0.1%, w/w), vitamin B-complex (0.01%) and moistened                1999; Kamini, Mala, & Puvanakrishnan, 1998; Miranda
with tap water containing 1% Tween-40.                              et al., 1999) under submerged conditions. However, few
   Recently, Ramachandran et al. (2004) reported the                researchers have investigated the synthesis of lipase by
use of coconut oil cake (COC) as a substrate for the pro-           yeasts using SSF technique. Among them, Rao,
duction of a-amylase by A. oryzae under SSF condi-                  Jayaraman, and Lakshmanan (1993) determined that
tions. Raw COC supported the growth of the culture,                 the C/N ratio of the medium is an important parameter
resulting in the production of 1372 U/gds a-amylase in              for lipase production by the yeast Candida rugosa.
24 h. Supplementation with 0.5% starch and 1% peptone                   Rivera-Muñoz, Tinoco-Valencia, Sanchez, and
to the substrate positively enhanced the enzyme synthe-             Farres (1991), Ohnishi, Yoshida, and Sekiguchi (1994),
sis producing 3388 U/gds, proving COC a promising                   Christen et al. (1995) and Benjamin and Pandey
substrate for a-amylase production.                                 (1996a, 1996b, 1997a, 1997b), compared SmF and SSF
 Sanromán / Journal of Food Engineering 76 (2006) 291–302
                           S.R. Couto, Ma. A.                                                                             295

systems for lipase production. All they found that en-             showed more stable properties: they had a higher
zyme yields were higher and stable in the latter.                  stability to pH and temperature and they were less
   Several factors can affect extracellular lipase produc-          affected by catabolic repression than pectinases pro-
tion such as pH, temperature, aeration and medium                  duced by SmF (Acuña-Arguelles et al., 1995).
composition. Furthermore, the presence of triglycerides
or fatty acids has been reported to increase lipolytic en-         2.3. Organic acids
zyme secretion by a certain number of microorganisms
(Marek & Bednarski, 1996). Therefore, in SSF the type                 Organic acids have been utilised for long time by the
of substrate could be used to enhance the production of            food industry as food additives and preservatives for
enzymes, as several food and agroindustrial wastes are             prevent deterioration and extending the shelf life of
rich in fatty acids, triglycerides and/or sugars.                  perishable food ingredients. Here, two common organic
   Dominguez, Costas, Longo, and Sanroman (2003)                   acids widely used on the food industry have been
have reported the great potential of food-agroindustrial           considered.
wastes (ground nut and barley bran) as support-sub-
strates for lipase production in solid state cultures of
                                                                   2.3.1. Lactic acid
the yeast Y. lipolytica, since they led to much higher
                                                                      Lactic acid fermentation has received extensive atten-
activities than those found using an inert support.
                                                                   tion since long time (Benninga, 1990; Vickroy, 1985). It
                                                                   has wide applications in food, pharmaceutical, leather
2.2.4. Pectinases
                                                                   and textile industries and as a chemical feed stock. It
   They constitute a heterogeneous group of enzymes
                                                                   has two enantiomers L(+) and D( ) of which L(+) is
that catalyse the degradation of pectins, which are the
                                                                   used by human metabolism due to the presence of L lac-
structural polysaccharides present in vegetable cells
                                                                   tate dehydrogenase and is preferred for food. Nowa-
and are responsible for maintaining the plant tissues
                                                                   days, lactic acid is in great demand due to its use as
integrity (Alkorta, Garbisu, Llama, & Serra, 1998). Pec-
                                                                   starting material to produce biodegradable polymers
tinases are widely used in the food industry to clarify
                                                                   used in medical, industrial and consumer products
fruit juices and wine, to improve oil extraction, to re-
                                                                   (Bohlmann & Yoshida, 2000; Gross & Kalra, 2002;
move the peel from citrus fruit, to increase the firmness
                                                                   Lichtfield, 1996; Malhotra, Raina, & Sanjay, 2000).
of several fruits and to degum fibres (Baker & Wicker,
                                                                      Soccol, Marin, Rimbault, and Labeault (1994) stud-
1996; Chang, Siddiq, Sinha, & Cash, 1994).
                                                                   ied the production of L(+)-lactic acid by Rhizopous ory-
   Commercial pectinase preparations are produced
                                                                   zae in solid-state conditions operating with sugarcane
from fungal microorganisms, mainly by Aspergillus
                                                                   bagasse as a support. They obtained a slightly higher
niger strains. The use of SSF for pectinase production
                                                                   productivity than in submerged cultivation. Also, Rich-
has been proposed using different solid agricultural
                                                                   ter and Träger (1994) investigated the L(+)-lactic acid
and agro-industrial residues as substrates such as wheat
                                                                   production by Lactobacillus paracasei in solid-state con-
bran (Castilho, Alves, & Medronho, 1999; Singh, Platt-
                                                                   ditions using sweet sorghum as a support. More re-
ner, & Diekmann, 1999), soy bran (Castilho et al., 2000),
                                                                   cently, Naveena, Altaf, Bhadrayya, Madhavendra, and
cranberry and strawberry pomace (Zheng & Shetty,
                                                                   Reddy (2005) and Naveena, Altaf, Bhadriah, and Reddy
2000), coffee pulp and coffee husk (Antier, Minjares,
                                                                   (2005) have reported the production of L(+) lactic acid
Roussos, & Viniegra-Gonzalez, 1993), husk (Antier,
                                                                   by Lactobacillus amylophilus GV6 under SSF conditions
Minjares, Roussos, Raimbault, & Viniegra-González,
                                                                   using wheat bran as both support and substrate.
1993; Boccas, Roussos, Gutierrez, Serrano, & Viniegra,
1994), cocoa (Schwan, Cooper, & Wheals, 1997), lemon
and orange peel (Garzón & Hours, 1991; Ismail, 1996;              2.4. Citric acid
Maldonado, Navarro, & Callieri, 1986), orange bagasse,
sugar cane bagasse and wheat bran (Martins, Silva, Da                 Citric acid is one of the most commonly used organic
Silva, & Gomes, 2002), sugar cane bagasse (Acuña-                 acids in food and pharmaceutical industries. The food
Arguelles, Gutierrez-Rojas, Viniegra-González, &                  industry is the largest consumer of citric acid, using al-
Favela-Torres, 1994) and apple pomace (Hours, Voget,               most 70% of the total production, followed by about
& Ertola, 1988a, 1988b). Also, Bai, Zhang, Qi, Peng,               12% for the pharmaceutical industry and 18% for other
and Li (2004) produced pectinase from A. niger by SSF              applications (Shah, Chattoo, Baroda, & Patiala, 1993).
using sugar beet pulp as a carbon source and wastewater            Its pleasant taste, high solubility and flavour-enhancing
from monosodium glutamate production as nitrogen                   properties have ensured its dominant position in the
and water source. This allowed not only reducing pro-              market. Although citric acid can be obtained by chemi-
duction costs but also decreasing the pollution source.            cal synthesis, the cost is much higher than using fermen-
   It was found that SSF was more productive than                  tation. It is mainly produced by SmF, by the filamentous
SmF and, in addition, the pectinases produced by SSF               fungus A. niger. Recently, in order to increase the
296                                         Sanromán / Journal of Food Engineering 76 (2006) 291–302
                           S.R. Couto, Ma. A.

efficiency of citric acid production using A. niger, SSF             the substrates, xanthan yields were comparable to those
has been studied as a potential alternative to SmF.                obtained from conventional submerged cultivation. In
   The production of citric acid depends strongly on an            addition, the products were analysed by NMR spectros-
appropriate strain and on operational conditions. Oxy-             copy, revealing a composition consistent with that of
gen level is an important parameter for citric acid fer-           commercial xanthan.
mentation. Several researchers (Pintado, Lonsane,
Gaime-Perraud, & Roussos, 1998; Prado et al., 2004)                2.6. SSF bioreactors
have studied the influence of forced aeration on citric
acid production and the metabolic activity of A. niger                The design of an efficient industrial-level reactor for
in SSF by respirometric analysis. They showed that                 SSF is of significance because SSF is more environmen-
citric acid production was favoured by a limited biomass           tally friendly than SmF. However, it shows considerable
production, which occurred with low aeration rates.                drawbacks such as transfer resistance, steep gaseous
Both works showed the feasibility of using the strain              concentration and heat gradients that develop within
A. niger for citric acid production by SSF.                        the medium bed, which may adversely affect solid-state
   Different agro-industrial residues such as apple                 fermentor performances (Ghildyal, Ramalaishna, Lon-
pomace, coffee husk, wheat straw, pineapple waste,                  sane, & Karantb, 1992; Lonsane, Saucedo-Castuneda,
mixed fruit, maosmi waste, cassava bagasse, banana,                & Raimbault, 1992; Sargantanis, Karim, Murphy,
sugar beet cosset and kiwi fruit peel have been investi-           Ryoo, & Tengerdy, 1992). Agitation and rotation in
gated for their potential to be used as substrates (Hang           SSF were often carried out to improve mass and heat
& Woodams, 1985; Khare, Krishana, & Gandhi, 1995;                  transfers, but the shearing force caused by agitation
Kumar, Jain, Shanker, & Srivastava, 2003a, 2003b;                  and rotation has adverse effects on medium porosity
Shojaosadati & Babaripour, 2002). In addition, SSF                 and disrupts fungal mycelia.
gave high citric acid yield without inhibition related to             There are four types of reactors to perform SSF pro-
presence of certain metal ions such as Fe2+, Mn2+,                 cesses and each in their own design tries to make condi-
Zn2+, etc. (Gutierrez-Rozas, Cordova, Auria, Revah,                tions more favourable for fermentation under solid state
& Favela-Torres, 1995), although Shankaranand and                  conditions. The bioreactors commonly used, which can
Lonsane (1994) reported that addition of these minerals            be distinguished by the type of aeration or the mixed
into the production media to a certain level enhanced              system employed, include the following:
citric acid production by 1.4–1.9 fold with respect to                Tray: It consists of flat trays. The substrate is spread
SmF. Therefore, SSF is a good way of using nutrient                onto each tray forming a thin layer, only a few centime-
rich solid waste as a substrate.                                   tres deep. The reactor is kept in a chamber at constant
                                                                   temperature through which humidified air is circulated
2.5. Xanthan gum                                                   (Fig. 1). The main disadvantage of this configuration
                                                                   is that numerous trays and large volume are required,
   Xanthan gum is a hetero-polysaccharide produced                 making it an unattractive design for large-scale produc-
industrially by the bacterium Xanthomonas campestris,              tion (Pandey, Soccol, Rodriguez-Leon, & Nigam, 2001).
fermenting commonly glucose or sucrose. It is the most                Packed-bed: It is usually composed of a column of
important microbial polysaccharide from the commer-                glass or plastic with the solid substrate retained on a per-
cial point of view, with a worldwide production of about           forated base. Through the bed of substrate humidified
30,000 tons per year, corresponding to a market of $408            air is continuously forced (Durand et al., 1993; Raimba-
million (Demain, 2000; Sutherland, 1998). This water-              ult, 1998; Rodrı́guez Couto, Rivela, Muñoz, &
soluble microbial polysaccharide gives aqueous solu-               Sanromán, 2000). It may be fitted with a jacket for
tions with several industrial applications in the food,            circulation of water to control the temperature during
cosmetic, textile and pharmaceutical industries due to             fermentation (Fig. 2). This is the configuration usually
their rheological properties. Because of these properties,         employed in commercial koji production. The main
they have been used as emulsifiers, as stabilisers and as           drawbacks associated with this configuration are: diffi-
texture enhancers in the food industry.                            culties in obtaining the product, non-uniform growth,
   Recently, the feasibility of this exopolysaccharide             poor heat removal and scale-up problems.
production using SSF has been reported by the group                   Horizontal drum: This design allows adequate aera-
of Stredansky and Conti (1999), Stredansky, Conti,                 tion and mixing of the substrate, whilst limiting the
Navarini, and Bertocchi (1999). X. campestris strains              damage to the inoculum or product. Mixing is per-
were cultivated on a great variety of solid substrates or          formed by rotating the entire vessel or by various agita-
by-products such as spent malt grains, apple pomace,               tion devices such as paddles and baffles (Domı́nguez,
grape pomace and citrus peels, easily available and                Rivela, Rodrı́guez Couto, & Sanromán, 2001; Nagel,
low cost substrates, in order to evaluate their ability to         Tramper, Bakker, & Rinzema, 2001a, Nagel, Tramper,
produce the exopolysaccharide xanthan. With most of                Bakker, & Rinzema, 2001b; Prado et al., 2004; Stuart,
 Sanromán / Journal of Food Engineering 76 (2006) 291–302
                                 S.R. Couto, Ma. A.                                                                                          297

                                                                              Gas exit
             Gas exit
                                                                                3 rpm
                                                                                                                        Support susbstrate

                                                                                                                           Culture medium level
                                                                         Sampling port             Air diffuser
                                                                                                                            Air inlet

                                                                         Fig. 3. Scheme of a horizontal drum bioreactor (humidified air;
                                                                Trays    mechanical agitation).

                          Solid substrate

                                                           Air inlet

   Fig. 1. Scheme of a tray bioreactor (passive aeration; static).

Mitchell, Johns, & Litster, 1999) (Fig. 3). Its main disad-
vantage is that the drum is filled to only 30% capacity,
otherwise mixing is inefficient.
   Fluidised bed: In order to avoid the adhesion and
aggregation of substrate particles, this design supplies
a continue agitation with forced air (Fig. 4). Although
the mass heat transfer, aeration and mixing of the sub-
strate is increased, damage to inoculum and heat
build-up through sheer forces may affect the final
product yield.
   The different disadvantages detected in the above-
mentioned bioreactor designs to perform SSF processes
have promoted the necessity of developing new bioreac-
tor configurations or modifying the already existing de-
signs. These bioreactor configurations should be able to
operate in continuous mode with high productivity for
prolonged periods of time without operational problems
as well as permit the scale-up of the process. Our re-
search group has been working in this field, resulting
                                                                         Fig. 4. Scheme of a fluidised-bed bioreactor (humidified air; pneu-
                                                                         matic agitation).

                                                                         in the design of a new bioreactor, called immersion bio-
                                                                         reactor. This bioreactor consists of a jacketed cylindrical
                                                                         glass vessel with a round bottom, inside which several
                                                                         wire mesh baskets filled with support colonised by the
                                                                         fungus are placed. They moved upwards and down-
                                                                         wards by means of a pneumatic system, remaining more
                                                                         time outside than inside the medium (Rivela, Rodrı́guez
                                                                         Couto, & Sanromán, 2000) (Fig. 5). It is noteworthy
                                                                         that this bioreactor configuration was also able to run
                                                                         in continuous mode without operational problems,
                                                                         attaining high ligninolytic enzyme activities (Rodriguez
                                                                         Couto, Barreiro, Rivela, Longo, & Sanroman, 2002).
                                                                            Different studies were carried out for the production
                                                                         of natural food and additives derived from micro-
 Fig. 2. Scheme of a packed-bed bioreactor (humidified air; static).      organisms in different bioreactor configurations. For
298                                                     Sanromán / Journal of Food Engineering 76 (2006) 291–302
                                       S.R. Couto, Ma. A.

                                                                                     A packed-bed bioreactor with four stages was con-
                                                                                  structed and operated for microbial production of citric
  Compressor       Pneumatic system
                                                                                  acid by A. niger using apple pomace as a substrate.
                                                                                  Under the optimised conditions, 124 g citric acid was
                                                       Gas exit
                                                                                  produced from 1 kg dry apple pomace with yield of
                                                                                  80% based on total sugar (Shojaosadati & Babaripour,
       Culture medium level

                                                                  Water cooling   3. Conclusion
           Mesh with substrate

                                                                                     Critical analysis of the literature shows that produc-
                                                                                  tion of relevant compounds for the food processing
                                 Sampling port
                                                 Air inlet
                                                                                  industry by SSF offers several advantages. It has been
                                                                                  well established that enzyme titres produced in SSF sys-
Fig. 5. Scheme of an immersion bioreactor (humidified air; mechanical              tems are much higher than the achieved in SmF ones.
agitation).                                                                       Although the reasons for this are not clear, this fact is
                                                                                  kept in mind while developing novel bioreactors for
                                                                                  SSF processes.
example, the production of aroma compounds by K.
marxianus grown on cassava bagasse in solid state fer-
mentation using packed bed reactors, testing two differ-                           Acknowledgments
ent aeration rates was studied by Medeiros et al. (2001).
Headspace analysis of the culture by gas chromatogra-                                The authors are grateful to Xunta de Galicia (local
phy showed the production of 11 compounds. The pre-                               government of Spain) for the financial support of the re-
dominant compounds were ethyl acetate, ethanol and                                search post of Susana Rodrı́guez Couto under the pro-
acetaldehyde. The fruity aroma was attributed to the                              gramme Isidro Parga Pondal.
productions of esters.
   Recently, Navarrete-Bolaños, Jiménez-Islas, Botello-
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