Abstract
Industrial enzymes are produced by submerged fermentation (SF) and by solid-state fermentation (SSF) to a lesser extent. Although SSF has several advantages, its scale-up is difficult. The role of physiological and genetic properties of microorganisms growing attached to surfaces could explain the advantages of SSF. Filamentous fungi are naturally adapted to growth on surfaces and in these conditions they show a particular physiological behavior which is different from that in SF; thus, they also form biofilms. Fermentation by filamentous fungal biofilms (FFB) is a homogeneous production system within a liquid environment based on the infrastructure of the SF process with the productive efficiency of the SSF. Enzyme production levels of FFB are much higher than those obtained in SF and they are also amenable of mixed fungal cultivation. Transcriptomic and proteomic tools are used to uncover the fundamental biological issues behind FFB. Several genes encoding cellulolytic enzymes are either differentially expressed or overexpressed in FFB. Moreover, our proteomic studies of Aspergillus niger biofilms compared to SF indicate that many intracellular proteins are either differentially expressed or overexpressed. Clinically important fungi like A. fumigatus also form biofilms when they infect lungs and recent studies demonstrate same gene expression features. These results support our hypothesis of cell adhesion and its role in the new schemes for improved fermentative production of industrial enzymes.
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Ramage, G., Rajendran, R., Gutiérrez-Correa, M., Jones, B., & Williams, C. (2011). FEMS Microbiol Lett, 324, 89–97.
Kolembrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S., & Palmer, R. J., Jr. (2002). Microbiol Mol Biol Rev, 66, 486–505.
Waters, C. M., & Bassler, B. L. (2005). Annu Rev Cell Dev Biol, 21, 319–346.
Bos, R., van der Mei, H. C., & Busscher, H. J. (1999). FEMS Microbiol Rev, 23, 179–230.
Yamada, K. M., & Geiger, B. (1997). Curr Opin Cell Biol, 9, 76–85.
Tanaka, A. & Kawamoto, T. (1999). in Manual of Industrial Microbiology and Biotechnology, 2nd ed. (Demain, A.L. & Davies, J.E., eds in-chief), ASM, Washington, pp. 94–102.
Groboillot, A., Boadi, D., Poncelet, D., & Neufeld, R. (1994). Crit Rev Biotechnol, 14, 75–102.
Norton, S., & Vuillemard, J.-C. (1994). Crit Rev Biotechnol, 14, 193–224.
Junter, G.-A., & Jouenne, T. (2004). Biotechnol Adv, 22, 633–658.
Gutiérrez-Correa, M., & Villena, G. K. (2010). In A. Pandey, C. R. Soccol, C. Larroche, E. Gnansounou, & P. Nigam-Singh (Eds.), Comprehensive Food Fermentation and Biotechnology, vol. 1 (pp. 183–227). New Delhi: Asiatech Publisher, Inc.
Gutiérrez-Correa, M., & Villena, G. K. (2003). Revista Peruana de Biología, 10, 113–124.
Doelle, H. W., Mitchell, D. A., & Rolz, C. E. (Eds.). (1992). Solid substrate cultivation. NY: Elsevier Science Pub.
Hölker, U., & Höfer, M. (2004). & Lenz, J. Appl Microbiol Biotechnol, 64, 175–186.
Krishna, C. (2005). Crit Rev Biotechnol, 25, 1–30.
Pandey, A. (2003). Biochem Eng J, 13, 81–84.
Soccol, C. R., & Vandenberghe, L. P. S. (2003). Biochem Eng J, 13, 205–218.
Suryanarayan, S. (2003). Biochem Eng J, 13, 189–195.
Park, J. H., Lee, S. Y., Kim, T. Y., & Kim, H. U. (2008). Trends Biotechnol, 26, 404–412.
Otero, J. M., & Nielsen, J. (2010). Biotechnol Bioeng, 105, 439–460.
Grimm, L. H., Kelly, S., Krull, R., & Hempel, D. C. (2005). Appl Microbiol Biotechnol, 69, 375–384.
Papagianni, M. (2004). Biotechnol Adv, 22, 189–259.
Kelly, S., Grimm, L. H., Hengstler, J., Schultheis, E., Krull, R., & Hempel, D. C. (2004). Bioprocess Biosyst Eng, 26, 315–323.
Ryoo, D., & Choi, C.-S. (1999). Biotechnol Lett, 21, 97–100.
Pazouki, M., & Panda, T. (2000). Bioprocess Eng, 22, 123–147.
Ma, H., Snook, L. A., Kaminskyj, S. G. W., & Dahms, T. E. S. (2005). Microbiology, 151, 3679–3688.
Hille, A., Neu, T. R., Hempel, D. C., & Horn, H. (2005). Biotechnol Bioeng, 92, 614–623.
El-Enshasy, H., Hellmuth, K., & Rinas, U. (1999). Appl Biochem Biotechnol, 81, 1–12.
Hamanaka, T., Higashiyama, K., Fujikawa, S., & Park, E. H. Y. (2001). Appl Microbiol Biotechnol, 56, 233–238.
Meyerhoff, J., & Bellgardt, R.-H. (1995). Bioprocess Eng, 12, 315–322.
Ghigo, J. M. (2003). Res Microbiol, 154, 1–8.
O’Toole, G., Kaplay, H. B., & Kolter, R. (2000). Annu Rev Microbiol, 54, 49–79.
Davey, M. E., & O’Toole, G. A. (2000). Microbiol Mol Biol Rev, 64, 847–867.
Fenchel, T. (2002). Science, 296, 1068–1071.
Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Nat Rev Microbiol, 2, 95–108.
Rosche, B., Li, X. Z., Hauer, B., Schmid, A., & Buehler, K. (2009). Trends Biotechnol, 26, 636–643.
Stoodley, P., Sauer, K., Davies, D. G., & Costerton, J. W. (2002). Annu Rev Microbiol, 56, 187–209.
Armstrong, E., Yan, L., Boy, K. G., Wright, P. C., & Burgess, J. G. (2001). Hydrobiologia, 461, 37–40.
Gilbert, P., & Lappin-Scott, H. (2000). Microbiol Today, 27, 136–137.
Watnick, P., & Kolter, R. (2000). J Bacteriol, 182, 2675–2679.
Blankenship, J. R., & Mitchell, A. P. (2006). Curr Opin Microbiol, 9, 588–594.
Reynolds, T. B., & Fink, G. R. (2001). Science, 291, 878–881.
Douglas, L. J. (2003). Trends Microbiol, 11, 30–36.
Chandrasekar, P. H., & Manavathu, E. K. (2008). Future Microbiol, 3, 19–21.
Villena, G.K., Moreno, P., & Gutiérrez-Correa, M. (2001). Agro-food-Industry Hi-Tech Jan./Feb., pp. 32–35.
Villena, G. K., & Gutiérrez-Correa, M. (2003). Revista Peruana de Biología, 10, 78–87.
Villena, G. K., & Gutiérrez-Correa, M. (2006). Lett Appl Microbiol, 43, 262–268.
Beauvais, A., Schmidt, C., Guadagnini, S., Roux, P., Perret, E., Henry, C., et al. (2007). Cell Microbiol, 9, 1588–1600.
Mowat, E., Butcher, J., Lang, S., Williams, C., & Ramage, G. (2007). J Med Microbiol, 56, 1205–1212.
Martinez, L. R., & Fries, B. C. (2010). Curr Fungal Infection Reports, 4, 266–275.
Ramage, G., Mowat, E., Jones, B., Williams, C., & Lopez-Ribot, J. (2009). Crit Rev Microbiol, 35, 340–355.
Wang, Z.-W., & Chen, S. (2009). Appl Microbiol Biotechnol, 83, 1–18.
Harding, M. W., Marques, L. L. R., Howard, R. J., & Olson, M. E. (2009). Trends Microbiol, 17, 475–480.
Villena, G. K., & Gutiérrez-Correa, M. (2007). Lett Appl Microbiol, 45, 231–237.
Villena, G. K., Fujikawa, T., Tsuyumu, S., & Gutiérrez-Correa, M. (2010). Bioresour Technol, 101, 1920–1926.
Bigerelle, M., Anselme, K., Dufresne, E., Hardouin, P., & Lost, A. (2002). Biomol Eng, 19, 79–83.
Cunliffe, D., Smart, C. A., Alexander, C., & Vulfson, E. N. (1999). Appl Environ Microbiol, 65, 4995–5002.
Dufrêne, Y. F. (2000). Biophys J, 78, 3286–3291.
Webb, J. S., Van der Mei, H. C., Nixon, M., Eastwood, I. M., Greenhalgh, M., Read, S. J., et al. (1999). Appl Environ Microbiol, 65, 3575–3585.
Gerin, P., Bellon-Fontaine, M. N., Asther, M., & Rouxhet, P. G. (1995). Biotechnol Bioeng, 47, 677–687.
Rouxhet, P. G., & Mozes, N. (1990). Water Sci Technol, 22, 1–16.
Linder, M. B., Szilvay, G. R., Nakari-Setälä, T., & Penttilä, M. E. (2005). FEMS Microbiol Rev, 29, 877–896.
Wösten, H. A. B. (2001). Annu Rev Microbiol, 55, 625–646.
Scholtmeijer, K., Wessels, J. G. H., & Wösten, H. A. B. (2001). Appl Microbiol Biotechnol, 56, 1–8.
Jensen, B. G., Andersen, M. R., Pedersen, M. H., Frisvad, J. C., & Søndergaard, I. (2010). BMC Res Notes, 3, 344. doi:10.1186/1756-0500-3-344.
Dupres, V., Alsteens, D., Andre, G., & Dufrêne, Y. F. (2010). Trends Microbiol, 18, 397–405.
Dague, E., Alsteens, D., Latgé, J.-P., & Dufrêne, Y. F. (2008). Biophys J, 94, 656–660.
Shaw, B. D., Carroll, G. C., & Hoch, H. C. (2006). Mycologia, 98, 186–194.
Hughes, H. B., Carzaniga, R., Rawlings, S. L., Green, J. R., & O’Connell, R. (1999). Microbiology, 145, 1927–1936.
Vesentini, D., Dickinson, D. J., & Murphy, R. J. (2005). Mycologia, 97, 1163–1170.
Villena, G. K. & Gutiérrez-Correa, M. (2007). Electronic Journal of Biotechnology 10, No.1, Issue of January 15, 2007 (doi: 10.2225/vol10-issue5-fulltext-2).
Apoga, D., Jansson, H.-B., & Tunlid, A. (2001). Mycol Res, 105, 1251–1260.
Gamarra, N. N., Villena, G. K., & Gutiérrez-Correa, M. (2010). Appl Microbiol Biotechnol, 87, 545–551.
Seidler, M. J., Salvenmoser, S., & Müller, F.-M. C. (2008). Antimicrob Agents Chemother, 52, 4130–4136.
Loussert, C., Schmitt, C., Prevost, M.-C., Balloy, V., Fadel, E., Philippe, B., et al. (2010). Cell Microbiol, 12, 405–410.
Osherov, N., & May, G. (2000). Genetics, 155, 647–656.
Tucker, S. L., & Talbot, N. J. (2001). Annu Rev Phytopathol, 39, 385–417.
Kim, Y.-K., Wang, Y., Liu, Z.-M., & Kolattukudy, P. E. (2002). Plant J, 30, 177–187.
Machida, M., Asai, K., Sano, M., Tanaka, T., Kumagai, T., Terai, G., et al. (2005). Nature, 438, 1157–1161.
Pel, H. J., de Winde, J. H., Archer, D. B., Dyer, P. S., Hofmann, G., Schaap, P. J., et al. (2007). Nat Biotechnol, 25, 221–231.
Sun, J., Lu, X., Rinas, U., & Zeng, A. P. (2007). Genome Biol, 8, R182. doi:10.1186/gb-2007-8-9-r182.
Andersen, M. R., Vongsangnak, W., Panagiotou, G., Salazar, M. P., Lehmann, L., & Nielsen, J. (2008). PNAS, 105, 4387–4392.
Kim, Y., Nandakumar, M. P., & Marten, M. R. (2008). Brief Funct Genomic Proteomic, 7, 87–94.
Andersen, M. R., & Nielsen, J. (2009). Fungal Genet Biol, 46, S180–S190.
McKelvey, S. M., & Murphy, R. A. (2010). J Ind Microbiol Biotechnol, 37, 455–469.
Akao, T., Gomi, K., Goto, K., Okazaki, N., & Akita, O. (2002). Curr Genet, 41, 275–281.
Ishida, H., Hata, Y., Kawato, A., Abe, Y., Suginami, K., & Imayasu, S. (2000). Curr Genet, 37, 373–379.
Iwashita, K. (2002). J Biosci Bioeng, 94, 530–535.
te Biesebeke, R., Ruijter, G., Rahardjo, Y. S. P., Hoogschagen, M. J., Heerikhuisen, M., Levin, A., et al. (2002). FEMS Yeast Res, 2, 245–248.
Tamano, K., Satoh, Y., Ishii, T., Terabayashi, Y., Ohtaki, S., Sano, M., et al. (2007). Biosci Biotechnol Biochem, 71, 926–934.
te Biesebeke, R., Levin, A., Sagt, C., Bartels, J., Goosen, T., Ram, A., et al. (2005). Mol Genet Genomics, 273, 33–42.
Vallim, M. A., Janse, B. J. H., Gaskell, J., Pizzirani-Kleiner, A. A., & Cullen, D. (1998). Appl Environ Microbiol, 64, 1924–1928.
Dai, Z., Mao, X., Magnuson, J. K., & Lasure, L. L. (2004). Appl Environ Microbiol, 70, 2474–2485.
Levin, A. M., de Vries, R. P., Conesa, A., de Bekker, C., Talon, M., Menke, H. H., et al. (2007). Eukaryot Cell, 6, 2311–2322.
Yuan, X.-L., van der Kaaij, R. M., van den Hondel, C. A. M. J. J., Punt, P. J., van der Maarel, M. J. E. C., Dijkhuizen, L., et al. (2008). Mol Genet Genomics, 279, 545–561.
Jørgensen, T.R., Goosen, T., van den Hondel, C.A.M.J.J., Ram, A.F.J., & Iversen, J.J.L. (2009). BMC Genomics 10: 44 (doi:10.1186/1471-2164-10-44).
Meyer, V., Arentshorst, M., Flitter, S. J., Nitsche, B. M., Kwon, M. J., Reynaga-Peña, C. G., et al. (2009). Eukaryot Cell, 8, 1677–1691.
Villena, G. K., Fujikawa, T., Tsuyumu, S., & Gutiérrez-Correa, M. (2009). Revista Peruana de Biología, 15, 97–102.
te Biesebeke, R., Levasseur, A., Boussier, A., Record, E., van den Hondel, C. A. M. J. J., & Punt, P. J. (2010). Fungal Biol, 114, 135–143.
Lee, B. N., & Adams, T. H. (1994). Genes Dev, 8, 641–651.
Seo, J. A., Guan, Y., & Yu, J. H. (2006). Genetics, 172, 1535–1544.
Breakspear, A., & Momany, M. (2007). Eukaryot Cell, 6, 1697–1700.
Rosén, S., Yu, J.-H., & Adams, T. H. (1999). EMBO J, 18, 5592–5600.
Miller, K. Y., Wu, J., & Miller, B. L. (1992). Genes Dev, 6, 1770–1782.
Gravelat, F. N., Doedt, T., Chiang, L. Y., Liu, H., Filler, S. G., Patterson, T. F., et al. (2008). Infect Immun, 76, 3632–3639.
Paris, S., Debeaupuis, J.-P., Crameri, R., Carey, M., Charlès, F., Prévost, M. C., et al. (2003). Appl Environ Microbiol, 69, 1581–1588.
Bruns, S., Seidler, M., Albrecht, D., Salvenmoser, S., Remme, N., Hertweck, C., et al. (2010). Proteomics, 10, 3097–3107.
Villena, G. K., Venkatesh, L., Yamazaki, A., Tsuyumu, S., & Gutiérrez-Correa, M. (2009). Revista Peruana de Biología, 16, 101–108.
Vashist, S., Frank, C. G., Jakob, C. A., & Ng, D. T. W. (2002). Mol Biol Cell, 21, 3955–3966.
Bencina, M., Legi, M., & Read, N. D. (2005). Mol Microbiol, 56, 268–281.
Moreno, A. B., Martínez del Pozo, A., & San Segundo, B. (2006). Appl Microbiol Biotechnol, 72.
Olmo, N., Turnay, J., Gonzalez de Buitrago, G., López de Silanes, I., Gavilanes, J. G., & Lizarbe, M. A. (2001). Eur J Biochem, 268, 2113–2123.
Makarov, A. A., & Ilinskaya, O. N. (2003). FEBS Lett, 540, 15–20.
Kirk, T. K., Croan, S., & Tien, M. (1986). Enzyme Microb Technol, 8, 27–32.
Kirkpatrick, N., & Palmer, J. M. (1987). Appl Microbiol Biotechnol, 27, 129–133.
Linko, S. (1988). Enzyme Microb Technol, 10, 410–417.
Venkatadri, R., & Irvine, R. L. (1993). Water Res, 27, 591–596.
Yang, F.-C., & Yu, J.-T. (1996). Bioprocess Eng, 15, 307–310.
Yang, F.-C., & Yu, J.-T. (1996). Bioprocess Eng, 16, 9–11.
Gerin, P. A., Asther, M., & Rouxhet, P. G. (1997). Enzyme Microb Technol, 20, 294–300.
Guimarães, C., Matos, C., Azeredo, J., Mota, M., & Oliveira, R. (2002). Biotechnol Lett, 24, 795–800.
Zheng, Z., & Obbard, J. P. (2002). J Biotechnol, 96, 241–249.
Govender, S., Jacobs, E. P., Leukes, W. D., & Pillay, V. L. (2003). Biotechnol Lett, 25, 127–131.
Govender, S., Jacobs, E. P., Leukes, W. D., Odhav, B., & Pillay, V. L. (2004). J Membr Sci, 238, 83–92.
Sheldon, M. S., & Small, H. J. (2005). J Membr Sci, 263, 30–37.
Yu, G., Wen, X., & Qian, Y. (2005). World J Microbiol Biotechnol, 21, 323–327.
Iqbal, M., Saeed, A., Edyvean, R. G. J., O’Sullivan, B., & Styring, P. (2005). Biotechnol Lett, 27, 1319–1323.
Ahmadi, M., Vahabzadeh, F., Bonakdarpour, B., Mehranian, M., & Mofarrah, E. (2006). World J Microbiol Biotechnol, 22, 119–127.
Karimi, A., Vahabzadeh, F., & Bonakdarpour, B. (2006). World J Microbiol Biotechnol, 22, 1251–1257.
Godongwana, B., Sheldon, M. S., & Solomons, D. M. (2007). J Membr Sci, 303, 86–99.
Ntwampe, S. K. O., Sheldon, M. S., & Volschenk, H. (2007). Afr J Biotechnol, 6, 1164–1170.
Ntwampe, S. K. O., Sheldon, M. S., & Volschenk, H. (2008). Brazilian J Chem Eng, 25, 649–664.
Sheldon, M. S., Mohammed, K., & Ntwampe, S. K. O. (2008). Enzyme Microb Technol, 42, 353–361.
Govender, S. (2011). Biotechnol Lett, 33, 263–271.
Pakshirajan, K., Sivasankar, A., & Sahoo, N. K. (2011). Appl Microbiol Biotechnol, 89, 1223–1232.
Sakurai, A., Kawamoto, S., Abarca, J. F., & Sakakibara, M. (2002). Biochem Eng J, 10, 47–53.
Wu, J., Xiao, Y.-Z., & Yu, H.-Q. (2005). Bioresour Technol, 96, 1357–1363.
Ryan, D. R., Russell, A. K., Leukes, W. D., Rose, P. D., & Burton, S. G. (1998). Desalination, 115, 303–306.
Sedarati, M. R., Keshavarz, T., Leontievsky, A. A., & Evans, C. S. (2003). Electronic Journal of Biotechnology 6, No.2, Issue of August 15; (doi: 10.2225/vol6-issue2-fulltext-7).
Nilsson, I., Möller, A., Mattiasson, B., Rubindamayugi, M. S. T., & Welander, U. (2006). Enzyme Microb Technol, 38, 94–100.
Ramsay, J., Shin, M., Wong, S., & Goode, C. (2006). J Ind Microbiol Biotechnol, 33, 791–795.
Alleman, B. C., Logan, B. E., & Gilbertson, R. L. (1995). Water Res, 29, 61–67.
Mtui, G., & Nakamura, Y. (2002). Biotechnol Lett, 24, 1743–1747.
Axelsson, J., Nilsson, U., Terrazas, E., Alvarez Aliaga, T., & Welander, U. (2006). Enzyme Microb Technol, 39, 32–37.
Shimokawa, T., Hirai, M., Shoda, M., & Sugano, Y. (2008). J Biosci Bioeng, 106, 481–487.
Lhomme, B., & Roux, J. C. (1992). Appl Microbiol Biotechnol, 37, 37–43.
Sun, Y., Li, Y.-L., Yang, H., Bai, S., & Hu, Z.-D. (1996). Biotechnol Tech, 10, 809–814.
Elibol, M., & Özer, D. (2000). Process Biochem, 36, 219–223.
Sankpal, N. V., Joshi, A. P., Sainkar, S. R., & Kulkarni, B. D. (2001). Process Biochem, 37, 395–403.
Yang, X., Wang, B., Cui, F., & Tan, T. (2005). Process Biochem, 40, 2095–2103.
Jasti, N., Rasmussen, M. L., Khanal, S. K., Pometto, A. L., III, & van Leeuwen, J. H. (2009). J Environ Eng, 135, 1106–1114.
Kutney, J. P., Berset, J.-D., Hewitt, G. M., & Singh, M. (1988). Appl Microbiol Biotechnol, 54, 1015–1022.
Kumar, P., & Satyanarayana, T. (2007). World J Microbiol Biotechnol, 23, 509–517.
Karhoot, J. M., Anderson, J. G., & Blain, J. A. (1987). Biotechnol Lett, 9, 471–474.
Endo, I., Nagamune, T., Kato, N., Nishimura, M., & Kobayashi, T. (1988). Bioprocess Eng, 3, 63–68.
de la Torre, M. A., Gomez-Alarcon, G., & Palacios, J. M. (1993). Appl Microbiol Biotechnol, 40, 408–415.
Meleigy, S. A., & Khalaf, M. A. (2009). Bioresour Technol, 100, 374–379.
Aleksieva, P., Tchorbanov, B., Michailova, L., & Nacheva, L. (2003). World J Microbiol Biotechnol, 19, 247–253.
Luke, A. K., & Burton, S. G. (2001). Enzyme Microb Technol, 29, 348–356.
Duff, J. (1988). Biotechnol Bioeng, 31, 345–348.
Haapala, R., Parkinnen, E., Suominen, P., & Linko, S. (1996). Enzyme Microb Technol, 18, 495–501.
Webb, C., Fukuda, H., & Atkinson, B. (1986). Biotechnol Bioeng, 28, 41–50.
Blain, J. A., Anderson, J. G., Todd, J. R., & Divers, M. (1979). Biotechnol Lett, 1, 269–274.
Anderson, J. G., Blain, J. A., Divers, M., & Todd, J. R. (1980). Biotechnol Lett, 2, 99–104.
Lee, Y. H., Lee, C. W., & Chang, H. N. (1989). Appl Microbiol Biotechnol, 30, 141–143.
Sanromán, A., Pintado, J., & Lema, J. M. (1994). Biotechnol Tech, 8, 389–394.
Heinrich, M., & Rehm, H. J. (1982). Eur J Appl Microbiol Biotechnol, 15, 88–92.
Sakurai, A., & Imai, H. (1992). J Ferment Bioeng, 73, 251–254.
Fujii, N., Yasuda, K., & Sakakibara, M. (1994). J Ferment Bioeng, 78, 389–393.
Sakurai, A., Itoh, M., Sakakibara, M., Saito, H., & Fujita, M. (1997). J Chem Technol Biotechnol, 70, 157–162.
Sakurai, A., Imai, H., Takenaka, Y., & Sakakibara, M. (1997). Biotechnol Bioeng, 56, 689–696.
Sakurai, A., Sakakibara, M., & Imai, H. (1997). In Z. Y. Shen, F. Ouyang, J. T. Yu, & Z. A. Cao (Eds.), Biochemical engineering: Marching toward the century of biotechnology, vol. 2 (pp. 786–789). Beijing: Tsuinghua University Press.
Papagianni, M., & Mattey, M. (2004). Process Biochem, 39, 1963–1970.
Sankpal, N. V., Joshi, A. P., & Kulkarni, B. D. (2001). Process Biochem, 36, 1129–1139.
Karaffa, L., & Kubicek, C. P. (2003). Appl Microbiol Biotechnol, 61, 189–196.
Kautola, H., Vassilev, N., & Linko, Y.-Y. (1989). Biotechnol Lett, 11, 313–318.
Kautola, H., Rymowicz, W., Linko, Y.-Y., & Linko, P. (1991). Appl Microbiol Biotechnol, 35, 154–158.
Iqbal, M., & Saeed, A. (2005). Lett Appl Microbiol, 40, 178–182.
Ju, N., & Wang, S. S. (1986). Appl Microbiol Biotechnol, 23, 311–314.
Vassilev, N. B., Vassileva, M. Ch., & Spassova, D. I. (1993). Appl Microbiol Biotechnol, 39, 285–288.
Fiedurek, J. (2001). Biotechnol Lett, 23, 1789–1792.
Marqués-Calvo, M. S. (2002). J Ind Microbiol Biotechnol, 29, 6–9.
Upreti, M. C., & Srivastava, R. B. (2003). Curr Sci, 84, 1399–1402.
Anderson, E. G., Blain, J. A., Marchetti, P., & Todd, J. R. (1981). Biotechnol Lett, 3, 451–454.
Sánchez, O., Ferrera, I., Vigués, N., García de Oteyza, T., Grimalt, J. O., & Mas, J. (2006). Int Microbiol, 9, 119–124.
Tsekova, K., & Ilieva, S. (2001). Appl Microbiol Biotechnol, 55, 636–637.
Dias, M. A., Lacerda, I. C. A., Pimentel, P. F., de Castro, H. F., & Rosa, C. A. (2002). Lett Appl Microbiol, 34, 46–50.
Ward, O. P., Qin, W. M., Dhanjoon, J., Ye, J., & Singh, A. (2006). Adv Appl Microbiol, 58, 1–75.
Punt, P. J., van Biezen, N., Conesa, A., Albers, A., Mangnus, J., & van den Hondel, C. (2002). Trends Biotechnol, 20, 200–206.
Liu, F., Li, W., Ridgway, D., Gu, T., & Moo-Young, M. (1998). Biotechnol Lett, 20, 539–542.
Papagianni, M., Joshi, N., & Moo-Young, M. (2002). J Ind Microbiol Biotechnol, 29, 259–263.
Talabardon, M., & Yang, S.-T. (2005). Biotechnol Prog, 21, 1389–1400.
Fiedurek, J., & Ilczuk, Z. (1991). World J Microbiol Biotechnol, 7, 379–384.
Mussatto, S. I., Rodrigues, L. R., & Teixeira, J. A. (2009). J Ind Microbiol Biotechnol, 36, 923–928.
Skowronek, M., & Fiedurek, J. (2006). Enzyme Microb Technol, 38, 162–167.
Murado, M. A., Siso, I. G., González, P., & Montemayor, I. (1994). Bioresour Technol, 48, 237–243.
Gawande, P. V., & Kamat, M. Y. (2000). World J Microbiol Biotechnol, 16, 111–112.
Kang, S. W., Kim, S. W., & Lee, J. S. (1995). Appl Biochem Biotechnol, 53, 101–106.
Hui, Y. S., Amirul, A. A., Yahya, A. R. M., & Azizan, M. N. M. (2010). World J Microbiol Biotechnol, 26, 79–84.
Nicolella, C., van Loosdrecht, M. C. M., & Heijnen, S. J. (2000). Trends Biotechnol, 18, 312–320.
Qureshi, N., Annous, B. A., Ezeji, T. C., Karcher, P., & Maddox, I. S. (2005). Microb Cell Fact, 4, 24. doi:10.1186/1475-2859-4-24.
Cheng, K.-C., Demirci, A., & Catchmark, J. M. (2010). Appl Microbiol Biotechnol, 87, 445–456.
Villena, G. K., & Gutiérrez-Correa, M. (2011). Afr J Biotechnol, 10(62), 13495–13504.
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This work was supported by grant Nº 072-FINCyT-PIN2008 from the National Program of Science and Technology of Peru (to G.K.V. and M.G.-C.).
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Gutiérrez-Correa, M., Ludeña, Y., Ramage, G. et al. Recent Advances on Filamentous Fungal Biofilms for Industrial Uses. Appl Biochem Biotechnol 167, 1235–1253 (2012). https://doi.org/10.1007/s12010-012-9555-5
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DOI: https://doi.org/10.1007/s12010-012-9555-5