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Fungi, a neglected component of acidophilic biofilms: do they have a potential for biotechnology?

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Abstract

Fungi from extreme environments, including acidophilic ones, belong to biotechnologically most attractive organisms. They can serve as a source of enzymes and metabolites with potentially uncommon properties and may actively participate within bioremediation processes. In respect of their biotechnological potential, extremophilic fungi are mostly studied as individual species. Nevertheless, microorganisms rarely live separately and they form biofilms instead. Living in biofilms is the most successful life strategy on the Earth and the biofilm is the most abundant form of life in extreme environments including highly acidic ones. Compared to bacterial fraction, fungal part of acidophilic biofilms represents a largely unexplored source of organisms with possible use in biotechnology and especially data on biofilms of highly acidic soils are missing. The functioning of the biofilm results from interactions between organisms whose metabolic capabilities are efficiently combined. When we look on acidophilic fungi and their biotechnological potential we should take this fact into account as well. The practical problem to be resolved in connection with extensive studies of exploitable properties and abilities of acidophilic fungi is the methodology of isolation of strains from the nature. In this respect, novel isolation techniques should be developed.

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References

  • Aguilera A, Olsson S, Puerte-Sánchez F (2016) Physiological and phylogenetic diversity of acidophilic eukaryotes. In: Quatrini R, Johnson DB (eds) Acidophiles: life in extremely acidic environment. Caister Academic Press, Norfolk, pp 107–118

    Chapter  Google Scholar 

  • Amaral-Zettler LA, Messerli MA, Laatsch AD, Smith PJS, Sorgin ML (2003) From genes to genomes: beyond biodiversity in Spain’s Rio Tinto. Biol Bull 204:205–209

    Article  CAS  Google Scholar 

  • Amezcua-Allieri M, Sánchez-Durán T, Aburto J (2017) Study of chemical and enzymatic hydrolysis of cellulosic material to obtain fermentable sugars. J Chem 2017:5680105

    Article  Google Scholar 

  • Armstrong RN (1999) Kinetic and chemical mechanism of epoxide hydrolase. Drug Metab Rev 31:71–86

    Article  CAS  Google Scholar 

  • Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  Google Scholar 

  • Baker BJ, Lutz MA, Dawson SC, Bond PL, Banfield JF (2004) Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl Environ Microbiol 70(10):6264–6271

    Article  CAS  Google Scholar 

  • Baker BJ, Tyson GW, Goosherst L, Banfield JF (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl Environ Microbiol 75(7):2192–2199

    Article  CAS  Google Scholar 

  • Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15(4):165–171

    Article  CAS  Google Scholar 

  • Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63(7):2495–2501

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boonen F, Vandamme A, Etoundi E, Pigneur L, Housen I (2014) Identification and charaterization of a novel multicopper oxidase from Acidomyces acidophilus with ferroxidase activity. Biochimie 102:37–46

    Article  CAS  Google Scholar 

  • Cánovas D, Durán C, Rodríguez N, Amils R, de Lorenzo V (2003) Testing the limits of biological tolerance to arsenic in a fungus isolated from the River Tinto. Environ Microbiol 5(2):133–138

    Article  Google Scholar 

  • Charoenpanich J (2013) Removal of acrylamide by microorganisms. In: Patil YB, Rao P (eds) Applied bioremediation—active and passive approaches. InTech, London, pp 101–121

    Google Scholar 

  • Chávez R, Fierro F, García-Rico RO, Vaca I (2015) Filamentous fungi from extreme environments as a promising source of novel bioactive secondary metabolites. Front Microbiol 6:903. https://doi.org/10.3389/fmicb.2015.00903

    Article  PubMed  PubMed Central  Google Scholar 

  • Črešnar B, Petrič Š (2011) Cytochrome P450 enzymes in the fungal kingdom. Biochim Biophys Acta 1814:29–35

    Article  Google Scholar 

  • Das BK, Roy A, Koschorreck M, Mandal SM, Wendt-Potthoff K, Bhattacharya J (2009) Occurrence and role of algae and fungi in acid mine drainage environment with special reference to metals and sulfate immobilization. Water Res 43:883–894

    Article  CAS  Google Scholar 

  • Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64(4):847–867

    Article  CAS  Google Scholar 

  • de Goes KCGP, da Silva JJ, Lovato GM, Iamanaka BT, Massi FP, Andrade DS (2017) Talaromyces sayulitensis, Acidiella bohemica and Penicillium citrinum in Brazilian oil shale by-products. Anton Leeuw Int J G 110(12):1637–1646

    Article  Google Scholar 

  • Deshmukh R, Khardenavis AA, Purohit HJ (2016) Diverse metabolic capacities of fungi for bioremediation. Indian J Microbiol 1:1. https://doi.org/10.1007/s12088-016-0584-6

    Article  CAS  Google Scholar 

  • Durairaj P, Hur JS, Yun H (2016) Versatile biocatalysis of fungal cytochrome P450 monooxygenases. Microb Cell Fact 15:125. https://doi.org/10.1186/s12934-016-0523-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durán C, Marín I, Amils R (1999) Specific metal sequestering acidophilic fungi. In: Amils R, Ballester A (eds) Biohydrometallurgy and the environment toward the mining of the 21st century, vol B. Elsevier, Amsterdam, pp 521–530

    Google Scholar 

  • Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbours. FEMS Microbiol Rev 36:990–1004

    Article  CAS  Google Scholar 

  • Ellouze M, Sayadi S (2016) White-rot fungi and their enzymes as a biotechnological tool for xenobiotic bioremediation. In: Saleh HEDM, Rahman ROA (eds) Management of hazardous wastes. InTech, London, pp 103–120

    Google Scholar 

  • Emmerton KS, Callaghan TV, Jones HE, Leake JR, Michelsen A, Read DJ (2001) Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytol 151:503–511

    Article  CAS  Google Scholar 

  • Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575

    Article  CAS  Google Scholar 

  • Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369. https://doi.org/10.3389/fmicb.2016.01369

    Article  PubMed  PubMed Central  Google Scholar 

  • Gostinčar C, Turk M (2012) Extremotolerant fungi as genetic resources for biotechnology. Bioengineered 3(5):293–297

    Article  Google Scholar 

  • Gostinčar C, Gunde-Cimerman N, Turk M (2012) Genetic resources of extremotolerant fungi: a method for identification of genes conferring stress tolerance. Biores Technol 111:360–367

    Article  Google Scholar 

  • Gryndler M, Hršelová H, Klír J, Kubát J, Votruba J (2003) Long-term fertilization affects the abundance of saprotrophic microfungi degrading resistant forms of soil organic matter. Folia Microbiol 48:76–82

    Article  CAS  Google Scholar 

  • Hölker U, Bend J, Pracht R, Tetsch L, Müller T, Höfer M, de Hoog GS (2004) Hortaea acidophila, a new acid-tolerant black yeast from lignite. Anton Leeuw Int J G 86:287–294

    Article  Google Scholar 

  • Horiike T, Yamashita M (2015) A new fungal isolate, Penidiella sp strain T9, accumulates the rare Earth element Dysprosium. Appl Env Microbiol 81(9):3062–3068

    Article  CAS  Google Scholar 

  • Hršelová H, Hujslová M, Gryndler M (2015) Genetic transformation of extremophilic fungi Acidea extrema and Acidothrix acidophila. Folia Microbiol 60(4):365–371

    Article  Google Scholar 

  • Hua H, Luo H, Bai Y, Wang K, Niu C, Huang H, Shi P, Wang C, Yang P, Yao B (2014) A thermostable glucoamylase from Bispora sp MEY-1 with stability over a broad pH range and significant starch hydrolysis capacity. PLoS One 9(11):e113581 10.1371/journal.pone.0113581

    Article  Google Scholar 

  • Hujslová M, Kubátová A, Kostovčík M, Kolařík M (2013) Acidiella bohemica gen. et sp. nov. and Acidomyces spp. (Teratosphaeriaceae), the indigenous inhabitants of extremely acidic soils in Europe. Fungal Divers 58:33–45

    Article  Google Scholar 

  • Hujslová M, Kubátová A, Kostovčík M, Blanchette RA, de Beer ZW, Chudíčková M, Kolařík M (2014) Three new genera of fungi from extremely acidic soils. Mycol Prog 13:819–831

    Google Scholar 

  • Hujslová M, Kubátová A, Bukovská P, Chudíčková M, Kolařík M (2017) Extremely acidic soils are dominated by species-poor and highly specific fungal communities. Microb Ecol 73:321–337

    Article  Google Scholar 

  • Ivarson KC, Morita H (1982) Single-cell protein production by the acidtolerant fungus Scytalidium acidophilum from acid hydrolysates of waste paper. Appl Env Microbiol 43(3):643–647

    CAS  Google Scholar 

  • Johnson BD (1998) MiniReview. Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317

    Article  CAS  Google Scholar 

  • Johnson DB (2014) Recent developments in microbiological approaches for securing mine wastes and for recovering metals from mine waters. Minerals 4:279–292

    Article  CAS  Google Scholar 

  • Joshi MH, Balamurugan P, Venugopalan VP, Rao TS (2011) Dense fouling in acid transfer pipelines by an acidophilic rubber degrading fungus. Biofouling 27(6):621–629

    Article  CAS  Google Scholar 

  • Kolařík M, Hujslová M, Vazquéz-Campos X (2015) Acidotolerant genus Fodinomyces (Ascomycota: Capnodiales) is a synonym of Acidiella. Czech Mycol 67:37–38

    Article  Google Scholar 

  • Krause S, Bremges A, Münch PC, McHardy AC, Gescher J (2017) Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms. Sci Rep 7:3289. https://doi.org/10.1038/s41598-017-03315-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusnin N, Syed MA, Ahmad SA (2015) Toxicity, pollution and biodegradation of acrylamide—a mini review. JOBIMB 3(2):6–12

    Google Scholar 

  • Lennon JT, Lehmkuhl BK (2016) A trait-based approach to bacterial biofilms in soil. Environ Microbiol 18(8):2732–2742

    Article  CAS  Google Scholar 

  • Luo H, Li J, Yang J, Wang H, Yang Y, Huang H, Shi P, Yuan T, Fan Y, Yao B (2009a) A thermophilic and acid stable family-10 xylanase from the acidophilic fungus Bispora sp. MEY-1. Extremophiles 13:849–857

    Article  CAS  Google Scholar 

  • Luo H, Wang Y, Wang H, Yang J, Yang Y, Huang H, Yang P, Bai Y, Shi P, Fan Y, Yao B (2009b) A novel highly acidic β-mannanase from acidophilic fungus Bispora sp. MEY-1: gene cloning and overexpression in Pichia pastoris. Appl Microbiol Biotechnol 82:453–461

    Article  CAS  Google Scholar 

  • Luo H, Wang Y, Li J, Wang H, Yang J et al (2009c) Cloning, expression and characterization of a novel acidic xylanase, XYL11B, from the acidophilic fungus Bispora sp. MEY-1. Enzyme Microb Tech 45:126–133

    Article  CAS  Google Scholar 

  • Luo H, Yang J, Yang P, Li J, Huang H et al (2010a) Gene cloning and expression of a new acidic family 7 endo-b-1,3-1,4-glucanase from the acidophilic fungus Bispora sp. MEY-1. Appl Microbiol Biotechnol 85:1015–1023

    Article  CAS  Google Scholar 

  • Luo H, Yang J, Li J, Shi P, Huang H, Bai Y, Fan Y, Yao B (2010b) Molecular cloning and characterization of the novel acidic xylanase XYLD from Bispora sp. MEY-1 that is homologous to family 30 glycosyl hydrolases. Appl Microbiol Biotechnol 86(6):1829–1839

    Article  CAS  Google Scholar 

  • Manson MM (1980) Epoxides—is there a human health problem? Br J Ind Med 37:317–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez P, Parada P (2016) Metabolomic approaches to the study of acidophiles. In: Quatrini R, Johnson DB (eds) Acidophiles: life in extremely acidic environments. Caister Academic Press, Norfolk, pp 249–262

    Chapter  Google Scholar 

  • Mathieu Y, Prosper P, Favier F, Harvengt L, Didierjean C, Jacquot J-P, Morel-Rouhier M, Gelhaye E (2013) Diversification of fungal specific class a glutathione transferases in saprotrophic fungi. PLoS One 8(11):e80298. https://doi.org/10.1371/journal.pone.0080298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M (2015) Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:475. https://doi.org/10.3389/fmicb.2015.00475

    Article  PubMed  PubMed Central  Google Scholar 

  • Mirete S, Morgante V, Gonzáles-Pastor JE (2017) Acidophiles: diversity and mechanisms of adaptation to acidic environments. In: Stan-Lotter H, Fendrihan S (eds) Adaption to microbial life to environmental extremes. Springer, Vienna, pp 227–251

    Chapter  Google Scholar 

  • Mosier AC, Justice NB, Bowen BP, Baran R, Thomas BC, Northen TR, Banfield JF (2013) Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics. MBIO 4(2):00484-12. https://doi.org/10.1128/mbio.00484-12

    Article  Google Scholar 

  • Mosier AC, Miller CS, Frischkorn KR, Ohm RA, Li Z, LaButti K, Lapidus A, Lipzen A, Chen C, Johnson J, Lindquist EA, Pan C, Hettich RL, Grigoriev IV, Singer SW, Banfield JF (2016) Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. Front Microbiol 7:238. https://doi.org/10.3389/fmicb.2016.00238

    Article  PubMed  PubMed Central  Google Scholar 

  • Neifar M, Maktouf S, Ghorbel RE, Jaouani A, Cherif A (2015) Extremophiles as source of novel bioactive compounds with industrial potential. In: Gupta VK, Tuohy MG, O᾽Donovan A, Lohani M (eds) Biotechnology of bioactive compounds: sources and applications. Wiley, Hoboken, pp 245–268

    Google Scholar 

  • Nigam PS (2013) Microbial enzymes with special characteristics for biotechnological applications. Biomolecules 3:597–611

    Article  Google Scholar 

  • Oggerin M, Tornos F, Rodriguez N, Pascual L, Amils R (2016) Fungal iron biomineralization in Rio Tinto. Minerals 6(2):37. https://doi.org/10.3390/min6020037

    Article  CAS  Google Scholar 

  • Purchase D (ed) (2016) Fungal applications in sustainable environmental biotechnology. Springer, Berlin

    Google Scholar 

  • Quatrini R, Johnson DB (2018) Microbiomes in extremely acidic environments: functionalities and interactions that allow survival and growth of prokaryotes at low pH. Curr Opin Microbiol 43:139–147

    Article  CAS  Google Scholar 

  • Řezáčová V, Baldrian P, Hršelová H, Larsen J, Gryndler M (2007) Influence of mineral and organic fertilization on soil fungi, enzyme activities and humic substances in a long-term field experiment. Folia Microbiol 52:415–421

    Article  Google Scholar 

  • Salinas AE, Wong MG (1999) Glutathione S-transferases—a review. Curr Med Chem 6:279–309

    CAS  PubMed  Google Scholar 

  • Selbmann L, de Hoog GS, Zucconi L, Isola D, Ruisi S, Gerrits van den Ende AHG, Ruibal C, De Leo F, Urzì C, Onofri S (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol 61:1–20

    Article  CAS  Google Scholar 

  • Selbmann L, Egidi E, Isola D, Onofri S, Zucconi L, de Hoog GS, Chinaglia S, Testa L, Tosi S, Balestrazzi A, Lantieri A, Compagno R, Tigini V, Varese GC (2013) Biodiversity, evolution and adaptation of fungi in extreme environments. Plant Bios 147(1):237–246

    Article  Google Scholar 

  • Sharma A, Kawarabayasi Y, Satyanarayana T (2012) Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16:1–19

    Article  CAS  Google Scholar 

  • Smit MS (2004) Fungal epoxide hydrolases: new landmarks in sequence-activity space. Trends Biotechnol 22(3):123–129

    Article  CAS  Google Scholar 

  • Stierle AA, Stierle DB (2017) Secondary metabolites of mine waste acidophilic fungi. In: Paterson R, Lima N (eds) Bioprospecting, topics in biodiversity and conservation. Springe, Berlin, pp 213–243

    Google Scholar 

  • Tetsch L, Bend J, Janßen M, Hölker U (2005) Evidence for functional laccases in the acidophilic ascomycete Hortaea acidophila and isolation of laccase-specific gene fragments. FEMS Microbiol Lett 245:161–168

    Article  CAS  Google Scholar 

  • Vazquéz-Campos X, Kinsela AS, Waite TD, Collins RN, Neilan BA (2014) Fodinomyces uranophilus gen. nov. sp. nov. and Coniochaeta fodinicola sp. nov., two uranium mine-inhabiting Ascomycota fungi from northern Australia. Mycologia 106(6):1073–1089

    Article  Google Scholar 

  • Wang H, Luo H, Bai Y, Wang Y, Yang P, Shi P, Zhang W, Fan Y, Yao B (2009) An acidophilic beta-galactosidase from Bispora sp. MEY-1 with high lactose hydrolytic activity under simulated gastric conditions. J Agric Food Chem 57(12):5535–5541

    Article  CAS  Google Scholar 

  • Wang H, Luo H, Li J, Bai Y, Huang H, Shi P, Fan Y, Yao B (2010) An alpha-galactosidase from an acidophilic Bispora sp. MEY-1 strain acts synergistically with beta mannanase. Bioresour Technol 101(21):8376–8382

    Article  CAS  Google Scholar 

  • Wu GX, Sorensen KB, Rodgers M, Zhan XM (2009) Microbial community associated with glucose-induced enhanced biological phosphorus removal. Water Sci Technol 60:2105–2113

    Article  CAS  Google Scholar 

  • Xu X, Zhang Y, Meng Q, Meng K, Zhang W, Zhou X, Luo H, Chen R, Yang P, Yao B (2013) Overexpression of a fungal β-mannanase from Bispora sp. MEY-1 in maize seeds and enzyme characterization. PLoS One 8(2):e56146. https://doi.org/10.1371/journal.pone.0056146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki A, Toyama K, Nakagiri A (2010) A new acidophilic fungus Teratosphaeria acidotherma (Capnodiales, Ascomycota) from a hot spring. Mycoscience 51:443–455

    Article  Google Scholar 

  • Yang J, Luo H, Li J, Wang K, Cheng H, Bai Y, Yuan T, Fan Y, Yao B (2011) Cloning, expression and characterization of an acidic endo-polygalacturonase from Bispora sp. MEY-1 and its potential application in juice clarification. Process Biochem 46(1):272–277

    Article  Google Scholar 

  • Zhang R, Bellenberg S, Neu TR, Sand W, Vera M (2016) The biofilm lifestyle of acidophilic metal/sulfur-oxidizing microorganisms. In: Rampelotto PH (ed) Biotechnology of extremophiles. Springer, Berlin, pp 177–213

    Chapter  Google Scholar 

  • Zhao J, Shi P, Luo H, Yang P, Zhao H, Bai Y, Huang H, Wang H, Yao B (2010) An acidophilic and acid-stable β-mannanase from Phialophora sp. P13 with high mannan hydrolysis activity under simulated gastric conditions. J Agric Food Chem 58:3184–3190

    Article  CAS  Google Scholar 

  • Zou J, Hallberg BM, Bergfors T, Oesch F, Arand M, Mowbray SL, Jones TA (2000) Structure of Aspergillus niger epoxide hydrolase at 1.8 Å resolution: implications for the structure and function of the mammalian microsomal class of epoxide hydrolases. Structure 8:111–122

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This text has been created within the frame of the project 17-09946S supported by the Czech Science Foundation. Lukáš Bystrianský was further supported by the student project of Internal grant agency SGS UJEP “Modification of polymer nanofiber textile” (J. E. Purkyně University in Ústí nad Labem). We thank Dr. Kofroňová (Institute of Microbiology ASCR, Czech Republic) for assistance with scanning electron microscopy.

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Authors and Affiliations

  1. Laboratory of Fungal biology, Institute of Microbiology ASCR, Vídeňská 1083, 14220, Prague, Czech Republic

    Martina Hujslová

  2. Department of Biology, Faculty of Science, Jan Evangelista Purkyně University in Ústí nad Labem, Za válcovnou 1000/8, 400 01, Ústí nad Labem, Czech Republic

    Lukáš Bystrianský, Oldřich Benada & Milan Gryndler

  3. Laboratory of Molecular Structure Characterization, Institute of Microbiology ASCR, Vídeňská 1083, 14220, Prague, Czech Republic

    Oldřich Benada

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  1. Martina Hujslová
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Hujslová, M., Bystrianský, L., Benada, O. et al. Fungi, a neglected component of acidophilic biofilms: do they have a potential for biotechnology?. Extremophiles 23, 267–275 (2019). https://doi.org/10.1007/s00792-019-01085-9

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