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Gongronella sp. w5 elevates Coprinopsis cinerea laccase production by carbon source syntrophism and secondary metabolite induction

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Abstract

When sucrose was used as the carbon source, the Basidiomycete Coprinopsis cinerea showed poor growth and low laccase activity in pure culture, but greatly enhanced the level of laccase activity (>1800 U/L) during coculture with the Mucoromycete Gongronella sp. w5. As a result, the mechanism of laccase overproduction in coculture was investigated by starting from clarifying the function of sucrose. Results demonstrated that Gongronella sp. w5 in the coculture system hydrolyzed sucrose to glucose and fructose by an intracellular invertase. Fructose rather than glucose was supplied by Gongronella sp. w5  as the readily available carbon source for C. cinerea, and contributed to an alteration of its growth behavior and a basal laccase secretion of 110.6 ± 3.3 U/L. On the other hand, separating Gongronella sp. w5 of C. cinerea by transfer into dialysis tubes yielded the same level of laccase activity as without separation, indicating that enhanced laccase production probably resulted from the metabolites in the fermentation broth. Further investigation showed that the ethyl acetate–extracted metabolites generated by Gongronella sp. w5 induced C. cinerea laccase production. One of the laccase-inducing compounds namely p-hydroxybenzoic acid (HBA) was purified and identified from the extract. When using HBA as the inducer and fructose as the carbon source in monoculture, C. cinerea observed similar high laccase activity to that in coculture, and zymograms revealed the same expression of laccase Lcc9 as the main and Lcc1 and Lcc5 as the minor enzymes. Overall, our experiments verified that Gongronella sp. w5 elevates Coprinopsis cinerea laccase production by carbon source syntrophism and secondary metabolite induction.

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References

  • Afri Y, Levasseur A, Record E (2013) Differential gene expression in Pycnoporus coccineus during interspecific mycelial interactions with different competitors. Appl Environ Microbiol 79:6626–6636

    Article  Google Scholar 

  • Alexandre G, Zhulin LB (2000) Laccases are widespread in bacteria. Trends Biotechnol 18:41–42

    Article  CAS  Google Scholar 

  • Armand D, Thivend S (1965) The production of phenolic acids by mycelia of hymenomycetes on a glucose medium. C R Acad Sci III 260:1472–1473

    CAS  Google Scholar 

  • Badalyan SM, Rapior S, Doko L, Lequang J, Jacob M, Serrano JJ, Andary C (1996) Chemical and pharmacological study of higher fungi. II. Comparative investigation of carpophores of some Nematoloma species: chemical composition and cultural characteristics. Mikol Fitopatol 30:79–86

  • Bader J, Mast-Gerlach E, Popović MK, Bajpai R, Stahl U (2010) Relevance of microbial coculture fermentations in biotechnology. J Appl Microbiol 109:371–387

    Article  CAS  Google Scholar 

  • Bahn YS, Xue C, Idnurm A, Rutherford JC, Heitman J, Cardenas ME (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69

    Article  CAS  Google Scholar 

  • Baldrian P (2004) Increase of laccase activities during interspecific interactions of white-rot fungi. FEMS Microbiol Ecol 50:245–253

    Article  CAS  Google Scholar 

  • Baldrian P (2006) Fungal laccases – occurrence and properties. FEMS Microbiol Rev 30:215–242

    Article  CAS  Google Scholar 

  • Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, Wolfender JL (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204

    Article  CAS  Google Scholar 

  • Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates. FEBS Lett 267(1):99–102

    Article  CAS  Google Scholar 

  • Cannatelli MD, Ragauskas AJ (2017) Two decades of laccases: advancing sustainability in the chemical industry. Chem Rec 17(1):122–140

    Article  CAS  Google Scholar 

  • Chen S, Ge W, Buswell JA (2004) Biochemical and molecular characterization of a laccase from the edible straw mushroom, Volvariella volvacea. Eur J Biochem 271(2):318–328

    Article  CAS  Google Scholar 

  • Chi Y, Hatakka A, Maijala P (2007) Can co-culturing of two white-rot fungi increase lignin degradation and the production of lignin-degrading enzymes? Int Biodeterior Biodegrad 59:32–39

    Article  CAS  Google Scholar 

  • Crowe JD, Olsson S (2001) Induction of laccase activity in Rhizoctonia solani by antagonistic Pseudomonas fluorescens strains and a range of chemical treatments. Appl Environ Microbiol 67:2088–2094

    Article  CAS  Google Scholar 

  • Dong YQ, Sun QY, Wang XJ, Zhang YL, Liu P, Xiao YZ, Fang ZM (2018) Complete genome of Gongronella sp. w5 provides insight into its relationship with plant. J Biotechnol 286:1–4. https://doi.org/10.1016/j.jbiotec.2018.08.022

  • Flores C, Vidal C, Trejo-Hernández MR, Galindo E, Serrano-Carreón L (2009) Selection of Trichoderma strains capable of increasing laccase production by Pleurotus ostreatus and Agaricus bisporus in dual cultures. J Appl Microbiol 106:249–257

    Article  CAS  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715–1719

    Article  CAS  Google Scholar 

  • Galhaup C, Wagner H, Barbara H, Haltrich D (2002) Increased production of laccase by the wood-degrading basidiomycete Trametes pubescens. Enzyme Microb Technol 30:529–536

    Article  CAS  Google Scholar 

  • Guo C, Zhao L, Wang F, Lu J, Ding Z, Shi G (2017) β-Carotene from yeasts enhances laccase production of Pleurotus eryngii var. ferulae in co-culture. Front Microbiol 8:1101

    Article  Google Scholar 

  • Hiscox J, Boddy L (2017) Armed and dangerous – chemical warfare in wood decay communities. Fungal Biol Rev 31(4):169–184

    Article  Google Scholar 

  • Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326

    Article  CAS  Google Scholar 

  • Iakovlev A, Stenlid J (2000) Spatiotemporal patterns of laccase activity in interacting mycelia of wood-decaying basidiomycete fungi. Microb Ecol 39:236–245

    CAS  PubMed  Google Scholar 

  • Jiang H, Ma Y, Chi Z, Liu GL, Chi ZM (2016) Production, purification, and gene cloning of a β-fructofuranosidase with a high inulin-hydrolyzing activity produced by a novel yeast Aureobasidium sp. P6 isolated from a mangrove ecosystem. Mar Biotechnol (NY) 18(4):500–510

    Article  CAS  Google Scholar 

  • Johannes C, Majcherczyk A (2000) Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl Environ Microbiol 66:524–528

    Article  CAS  Google Scholar 

  • Kilaru S, Hoegger PJ, Kües U (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50(1):45–60

  • Klonowska A, Petit JL, Tron T (2001) Enhancement of minor laccases production in the basidiomycete Marasmius quercophilus C30. FEMS Microbiol Lett 200:25–30

    Article  CAS  Google Scholar 

  • Kobayashi DY, Crouch JA (2009) Bacterial/fungal interaction: from pathogens to mutualistic endosymbionts. Annu Rev Phytopathol 47:63–82

    Article  CAS  Google Scholar 

  • Kudanga T, Nemadziva B, Le Roes-Hill M (2017) Laccase catalysis for the synthesis of bioactive compounds. Appl Microbiol Biotechnol 101(1):13–33

    Article  CAS  Google Scholar 

  • Kües U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353

    Article  Google Scholar 

  • Kües U, Rühl M (2011) Multiple multi-copper oxidase gene families in basidiomycetes - what for? Curr Genomics 12:72–94

    Article  Google Scholar 

  • Lakshmanan D, Sadasivan C (2016) Trichoderma viride laccase plays a crucial role in defense mechanism against antagonistic organisms. Front Microbiol 7:741. https://doi.org/10.3389/fmicb.2016.00741

  • Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60(3):727–740

    Article  CAS  Google Scholar 

  • Li P, Wang H, Liu G, Li X, Yao J (2011) The effect of carbon source succession on laccase activity in the co-culture process of Ganoderma lucidum and a yeast. Enzym Microb Technol 48:1–6

    Article  CAS  Google Scholar 

  • Marques WL, Raghavendran V, Stambuk BU, Gombert AK (2016) Sucrose and Saccharomyces cerevisiae: a relationship most sweet. FEMS Yeast Res 16(1):fov107

    Article  Google Scholar 

  • Mata G, Murrieta Hernández DM, Iglesias Andreu LG (2005) Changes in lignocellulolytic enzyme activites in six Pleurotus spp. strains cultivated on coffee pulp in confrontation with Trichoderma spp. World J Microbiol Biotechnol 21:143–150

    Article  CAS  Google Scholar 

  • Moore D (1969) Sources of carbon and energy used by Coprinus lagopus sensu Buller. J Gen Microbiol 58:49–56

    Article  CAS  Google Scholar 

  • Pan K, Zhao N, Yin Q, Zhang T, Xu X, Fang W, Hong Y, Fang Z, Xiao Y (2014) Induction of laccase Lcc9 from Coprinopsis cinerea by fungal coculture and its application on indigo dye decolorization. Bioresour Technol 162:45–52

    Article  CAS  Google Scholar 

  • Periasamy R, Palvannan T (2010) Optimization of laccase production by Pleurotus ostreatus IMI 395545 using the Taguchi DOE methodology. J Basic Microbiol 50(6):548–556

    Article  CAS  Google Scholar 

  • Petersen TN, Brunak S, Heijne GV, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786

    Article  CAS  Google Scholar 

  • Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genomics 12:104–112

    Article  CAS  Google Scholar 

  • Rühl M, Majcherczyk A, Kües U (2013) Lcc1 and Lcc5 are the main laccases secreted in liquid cultures of Coprinopsis cinerea strains. Antonie van Leeuwenhoek 103(5):1029–1039

  • Savoie JM, Mata G, Billette C (1998) Extracellular laccase production during hyphal interactions between Trichoderma sp. and Shiitake, Lentinula edodes. Appl Microbiol Biotechnol 49:589–593

    Article  CAS  Google Scholar 

  • Savoie JM, Mata G, Mamoun M (2001) Variability in brown line formation and extracellular laccase production during interaction between white-rot basidiomycetes and Trichoderma harzianum biotype Th2. Mycologia 93:243–248

    Article  CAS  Google Scholar 

  • Schroeckh V, Scherlach K, Nützmann HW, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106:14558–14563

    Article  CAS  Google Scholar 

  • Sjaarda CP, Abubaker KS, Castle AJ (2015) Induction of lcc2 expression and activity by Agaricus bisporus provides defence against Trichoderma aggressivum toxic extracts. Microbe Biotechnol 8:918–929. https://doi.org/10.1111/1751-7915.12277

    Article  CAS  Google Scholar 

  • Stajich JE, Wilke SK, Ahren D, Au CH, Birren BW, Borodovsky M, Burns C, Canbäck B, Casselton LA, Cheng CK, Deng J, Dietrich FS, Fargo DC, Farman ML, Gathman AC, Goldberg J, Guigo R, Hoegger PJ, Hooker JB, Huggins A, James TY, Kamada T, Kilaru S, Kodira C, Kües U, Kupfer D, Kwan HS, Lomsadze A, Li W, Lilly WW, Ma LJ, Mackey AJ, Manning G, Martin F, Muraguchi H, Natvig DO, Palmerini H, Ramesh MA, Rehmeyer CJ, Roe BA, Shenoy N, Stanke M, Ter-Hovhannisyan V, Tunlid A, Velagapudi R, Vision TJ, Zeng Q, Zolan ME, Pukkila PJ (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci U S A 107(26):11889–11894

  • Tavares APM, Coelho MAZ, Coutinho JAP, Xavier A (2005) Laccase improvement in submerged cultivation: induced production and kinetic modelling. J Chem Technol Biotechnol 80(6):669–676

    Article  Google Scholar 

  • Ujor VC, Adukwu EC, Okonkwo CC (2018) Fungal wars: the underlying molecular repertoires of combating mycelia. Fungal Biol 122(4):191–202

    Article  Google Scholar 

  • Van der Nest MA, Steenkamp ET, McTaggart AR, Trollip C, Godlonton T, Sauerman E, Roodt D, Naidoo K, Coetzee MP, Wilken PM, Wingfield MJ, Wingfield BD (2015) Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose. BMC Evol Biol 15:273

    Article  Google Scholar 

  • Vargas WA, Mandawe JC, Kenerley CM (2009) Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol 151:792–808

    Article  CAS  Google Scholar 

  • Vargas WA, Crutcher FK, Kenerley CM (2011) Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol 189:777–789

    Article  CAS  Google Scholar 

  • Velázquez-Cedeño M, Farnet AM, Mata G, Savoie JM (2008) Role of Bacillus spp. in antagonism between Pleurotus ostreatus and Trichoderma harzianum in heat-treated wheat-straw substrates. Bioresour Technol 99(15):6966–6973

    Article  Google Scholar 

  • Wahl R, Wippel K, Goos S, Kämper J, Sauer N (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8(2):e1000303

  • Wang H, Yu G, Li P, Gu Y, Li J, Liu G, Yao J (2009) Overproduction of Trametes versicolor laccase by making glucose starvation using yeast. Enzym Microb Technol 45:146–149

    Article  CAS  Google Scholar 

  • Wang H, Peng L, Ding Z, Wu J, Shi G (2015) Stimulated laccase production of Pleurotus ferulae JM301 fungus by Rhodotorula mucilaginosa yeast in co-culture. Process Biochem 50(6):901–905

    Article  CAS  Google Scholar 

  • Wei F, Hong Y, Liu J, Yuan J, Fang W, Peng H, Xiao Y (2010) Gongronella sp. induces overproduction of laccase in Panus rudis. J Basic Microbiol l50:98–103

    Article  Google Scholar 

  • Xiao YZ, Tu XM, Wang J, Zhang M, Cheng Q, Zeng WY, Shi YY (2003) Purification, molecular characterization and reactivity with aromatic compounds of a laccase from basidiomycete Trametes sp. strain AH28-2. Appl Microbiol Biotechnol 60(6):700–707

    Article  CAS  Google Scholar 

  • Xiao YZ, Chen Q, Hang J, Shi YY, Wu J, Hong YZ, Wang YP (2004) Selective induction, purification and characterization of a laccase isozyme from the basidiomycete Trametes sp. AH28-2. Mycologia 96:26–35

    Article  CAS  Google Scholar 

  • Xie N, Chapeland-Leclerc F, Silar P, Ruprich-Robert G (2014) Systematic gene deletions evidences that laccases are involved in several stages of wood degradation in the filamentous fungus Podospora anserina. Environ Microbiol 16:141–161

    Article  CAS  Google Scholar 

  • Yang J, Li W, Ng TB, Deng X, Lin J, Ye X (2017) Laccases: production, expression regulation, and applications in pharmaceutical biodegradation. Front Microbiol 8:832. https://doi.org/10.3389/fmicb.2017.00832

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451

    Article  CAS  Google Scholar 

  • Zhang H, Hong YZ, Xiao YZ, Yuan J, Tu XM, Zhang XQ (2006) Efficient production of laccases by Trametes sp. AH28-2 in cocultivation with a Trichoderma strain. Appl Microbiol Biotechnol 73:89–94

    Article  CAS  Google Scholar 

  • Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME J 12:2339–2351. https://doi.org/10.1038/s41396-018-0171-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong Z, Li L, Chang P, Xie H, Zhang H, Igarashi Y, Li N, Luo F (2017) Differential gene expression profiling analysis in Pleurotus ostreatus during interspecific antagonistic interactions with Dichomitus squalens and Trametes versicolor. Fungal Biol 121(12):1025–1036

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Prof. Patricia J. Pukkila (University of North Carolina, Chapel Hill, USA) for providing the strain C. cinerea strain Okayama 7 (#130), and to Jingjing Wang, Nannan Zhao, and Prof. Xiaotang Wang for suggestions.

Funding

This work was supported by grants from the Natural Sciences Foundation of China (31870098, 31300044), the Chinese Scholarship Council (201706505019) for a research stay of ZF in Goettingen, and the National Natural Science Foundation of Anhui Province (1308085QC46).

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  1. Jun Hu and Yinliang Zhang contributed equally to this work

Authors and Affiliations

  1. School of Life Sciences, Anhui University, Hefei, 230601, Anhui, China

    Jun Hu, Yinliang Zhang, Yong Xu, Qiuying Sun, Juanjuan Liu, Wei Fang, Yazhong Xiao & Zemin Fang

  2. Anhui Key Laboratory of Modern Biomanufacturing, Hefei, 230601, Anhui, China

    Jun Hu, Yinliang Zhang, Yong Xu, Qiuying Sun, Juanjuan Liu, Wei Fang, Yazhong Xiao & Zemin Fang

  3. Anhui Provincial Engineering Technology Research Center of Microorganisms and Biocatalysis, Hefei, 230601, Anhui, China

    Jun Hu, Yinliang Zhang, Yong Xu, Qiuying Sun, Juanjuan Liu, Wei Fang, Yazhong Xiao & Zemin Fang

  4. Molecular Wood Biotechnology and Technical Mycology, Büsgen-Institute, University of Goettingen, Büsgenweg 2, 37077, Goettingen, Germany

    Ursula Kües

  5. Goettingen Center for Molecular Biosciences (GZMB), University of Goettingen, 37077, Goettingen, Germany

    Ursula Kües

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Hu, J., Zhang, Y., Xu, Y. et al. Gongronella sp. w5 elevates Coprinopsis cinerea laccase production by carbon source syntrophism and secondary metabolite induction. Appl Microbiol Biotechnol 103, 411–425 (2019). https://doi.org/10.1007/s00253-018-9469-4

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