Application of solid-state fermentation to food industry-A review
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Journal of Food Engineering 76 (2006) 291–302 www.elsevier.com/locate/jfoodeng Application of solid-state fermentation to food industry—A review a,b Susana Rodrı́guez Couto , Ma Ángeles Sanromán a,* a Department of Chemical Engineering, Isaac Newton Building, University of Vigo, Lagoas Marcosende, 36310 Vigo, Spain b 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 Abstract 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 described. 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: firstname.lastname@example.org (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. doi:10.1016/j.jfoodeng.2005.05.022
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 184.108.40.206) 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 220.127.116.11) 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 18.104.22.168) 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 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, 2002). 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- Alvarez, Rico-Martı́nez, and Paredes-López (2004) have References employed a modular rotating drum bioreactor (equipped with inlet air injection, variable speed pumps, Acuña-Arguelles, M. E., Gutierrez-Rojas, M., Viniegra-González, G., humidiﬁer, and gas analyser) for xanthophylls extrac- & Favela-Torres, E. (1994). Eﬀect of water activity on exo- pectinase production by Aspergillus niger CH4 on solid state tion from marigold ﬂowers. Marigold extracts have been fermentation. Biotechnology Letters, 16, 23–28. commercialised internationally and are used as additives Acuña-Arguelles, M. E., Gutierrez-Rojas, M., Viniegra-González, G., for poultry feed, as they provide bright colours in egg & Favela-Torres, E. (1995). Production and properties of three yolks, skin, and fatty tissues. For this reason, they are pectinolytic activities produced by Aspergillus niger in submerged used as an additive in several food and pharmaceutical and solid-state fermentation. Applied and Microbiology Biotech- nology, 43, 808–814. industries. Based on experimental design strategies, opti- Alkorta, I., Garbisu, G., Llama, M. J., & Serra, J. L. (1998). Industrial mum operation values were determined for aeration, applications of pectic enzymes: a review. Process Biochemistry, 33, moisture, agitation and marigold-to-inoculum ratio in 21–28. SSF of marigold ﬂowers by mixed culture of three Antier, P., Minjares, A., Roussos, S., Raimbault, M., & Viniegra- microorganisms (Flavobacterium IIb, Acinetobacter anit- González, G. (1993). Pectinase-hyperproducing mutants of Asper- gillus niger C28B25 for solid-state fermentation of coﬀee pulp. ratus, and Rhizopus nigricans), leading to a xanthophylls Enzyme and Microbial Technology, 15, 254–260. yield of 17.8-g/kg dry weight. This value represented a Antier, P., Minjares, A., Roussos, S., & Viniegra-Gonzalez, G. (1993). 65% increase in relation to the control. New approach for selecting pectinase producing mutants of Milagres, Santos, Piovan, and Roberto (2004) have Aspergillus niger well adapted to solid state fermentation. Biotech- shown that Thermoascus aurantiacus was able to pro- nology Advances, 11, 429–440. Auria, R., Palacios, J., & Revah, S. (1992). Determination of the duce a high level of thermostable xylanase when sugar interparticular eﬀective diﬀusion coeﬃcient for CO2 and O2 in solid cane bagasse was used as a substrate in a glass-column state fermentation. Biotechnology Bioengineering, 39, 898–902. reactor with forced aeration. The airﬂow rate had a sig- Babu, K. R., & Satyanarayana, T. (1995). a-Amylase production by niﬁcant eﬀect on enzyme activity, whereas initial mass of thermophilic Bacillus coagulans in solid state fermentation. Process bagasse had none. The highest yield of xylanase Biochemistry, 30, 305–309. Bai, Z. H., Zhang, H. X., Qi, H. Y., Peng, X. W., & Li, B. J. (2004). (1597 U/g) was obtained operating in the bioreactor at Pectinase production by Aspergillus niger using wastewater in solid the optimal conditions: airﬂow rate (6 l/h g) and sub- state fermentation for eliciting plant disease resistance. Bioresource strate (8 g). Technology, 95, 49–52.
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