Abstract
Multi-copper oxidases (MCOs) are enzymes accepting a wide range of organic and inorganic substrates. MCOs (including laccases) in lignolytic white and brown rot fungi are represented by multiple members of gene families that have different roles in fungal sexual and asexual development as well as in lignin degradation. Differential regulation of the two laccases (Lcc1 and Lcc2) and four laccase-like (Mco1 through Mco4) MCOs in S. commune were analyzed and correlated with morphogenetic processes during sexual development. Transcripts of lcc2 were found to accumulate in the monokaryotic mycelia and showed up-regulation during the dikaryotic phase. Gene mco2 was up-regulated in the primordial and fruiting phases and mco3 was expressed mainly in fruiting bodies. Enzymatic activities were indeed higher in dikaryons and during fruiting. Regulatory promoter elements were determined to be in agreement with stress responses for the remaining genes. Homology-based protein models were used to identify subfamily associations via a similar potential domain structure, including predicted sites of post-translation modifications. Thus, we could assign different functions in development to members of this protein family.
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Albarouki E, Deising HB (2013) Infection structure-specific reductive iron assimilation is required for cell wall integrity and full virulence of the maize pathogen Colletotrichum graminicola. Mol Plant Microbe Interact 26:695–708
Ander P, Eriksson KE (1976) The importance of phenol oxidase activity in lignin degradation by the white rot fungus Sporotrichum pulverulentum. Arch Microbiol 109:1–8
Arora DS, Sharma RK (2010) Ligninolytic fungal laccases and their biotechnological applications. Appl Biochem Biotechnol 160:1760–1788
Baldrian P (2006) Fungal laccases- occurrence and properties. FEMS Microbiol Rev 30:215–242
Bermek H, Li K, Eriksson KE (1998) Laccase-less mutants of the white rot fungus Pycnoporus cinnabarinus cannot delignify kraft pulp. J Biotechnol 66:117–124
Bradford M (1976) A Rapid and Sensitive Method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chen S, Ge W, Buswell JA (2004) Biochemical and molecular characterization of a laccase from the edible straw mushroom, Volvariella volvacea. Eur J Biochem 271:318–328
De Tullio MC, Guether M, Balestrini R (2013) Ascorbate oxidase is the potential conductor of a symphony of signaling pathways. Plant Signal Behav 8:8
De Vries OMH, Kooistra WHCF, Wessels GM (1986) Formation of extracellular laccase by Schizophyllum commune dikaryon. J Gen Microbiol 132:2817–2826
Eggert C, LaFayette PR, Temp U, Eriksson KEL, Dean JFD (1998) Molecular analysis of a laccase gene from the white rot fungus Pycnoporus cinnabarinus. Appl Environ Microbiol 64:1766–1772
Faraco V, Giardina P, Sannia G (2003) Metal-responsive elements in Pleurotus ostreatus laccase gene promoters. Microbiology 149:2155–2162
Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010) Laccases: a never-ending story. Cell Mol Life Sci 67:369–385
Hellman NE, Gitlin JD (2002) Ceruloplasmin metabolism and function. Annu Rev Nutr 22:439–458
Hoegger PJ, Kilaru S, James TY, Thacker JR, Kues U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326
Hu DD, Zhang RY, Zhang GQ, Wang HX, Ng TB (2011) A laccase with antiproliferative activity against tumor cells from an edible mushroom, white common Agrocybe cylindracea. Phytomedicine 18:374–379
Jung WH, Hu G, Kuo W, Kronstad JW (2009) Role of ferroxidases in iron uptake and virulence of Cryptococcus neoformans. Eukaryot Cell 8:1511–1520
Kallio JP, Gasparetti C, Andberg M, Boer H, Koivula A, Kruus K, Rouvinen J, Hakulinen N (2011) Crystal structure of an ascomycete fungal laccase from Thielavia arenaria – common structural features of asco-laccases. FEBS J 278:2283–2295
Kelley LA, Sternberg MJE (2009) A case study using the Phyre server. Nat Protoc 4:363–371
Kothe E (1996) Tetrapolar fungal mating types: Sexes by the thousands. FEMS Microbiol Rev 18:65–87
Kües U, Rühl M (2011) Multiple multi-copper oxidase gene families in basidiomycetes - what for? Curr Genomics 12:72–94
Kumar SVS, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394
Kunamneni A, Ballesteros A, Plou FJ, Alcalde M (2007) Fungal laccase – a versatile enzyme for biotechnological applications. In: Mendez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formex, Badajoz, Spain, p 233–245
Largeteau ML, Latapy C, Minvielle N, Regnault-Roger C, Savoie JM (2010) Expression of phenol oxidases and heat shock genes during the development of Agaricus bisporus fruiting bodies, healthy and infected by Lecanicillium fungicola. Appl Microbiol Biotechnol 85:1499–1507
Larrondo LF, Salas L, Melo F, Vicuna R, Cullen D (2003) A novel extracellular multicopper oxidase from Phanerochaete chrysosporium with ferroxidase activity. Appl Environ Microbiol 69:6257–6263
Leatham GF, Stahmann MA (1981) Studies on the laccase of Lentinula edodes: Specificity localization and association with the development of fruiting bodies. J Gen Microbiol 125:147–157
Leonard TJ, Phillips LE (1973) Study of phenoloxidase activity during the reproductive cycle in Schizophyllum commune. J Bacteriol 114:7–10
Leonowicz A, Cho N, Luterek J, Wilkolazka A, Wojtas-wasilewska M, Matuszewska A, Hofrichter M, Wesenberg D, Rogalski J (2001) Fungal laccase: properties and activity on lignin. J Basic Microbiol 41:185–227
Lettera V, Piscitelli A, Leo G, Birolo L, Pezzella C, Sannia G (2010) Identification of a new member of Pleurotus ostreatus laccase family from mature fruiting body. Fungal Biol 114:724–730
Linke D, Bouws H, Peters T, Nimtz M, Berger RG, Zorn H (2005) Laccases of Pleurotus sapidus: characterization and cloning. J Agric Food Chem 53:9498–9505
Marzluf GA (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiol Mol Biol Rev 61:17–32
Messerschmidt A, Ladenstein R, Huber R et al (1992) Refined crystal structure of ascorbate oxidase at 1.9 A resolution. J Mol Biol 224:179–205
Morozova OV, Shumakovich GP, Gorbacheva MA, Shleev SV, Yaropolov AI (2007) Blue laccases. Biochem Mosc 72:1136–1150
Nakade K, Watanabe H, Sakamoto Y, Sato T (2011) Gene silencing of the Lentinula edodes lcc1 gene by expression of a homologous inverted repeat sequence. Microbiol Res 166:484–493
Nakamura K, Go N (2005) Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci 62:2050–2066
Ohga S, Cho NS, Thurston CF, Wood DA (2000) Transcriptional regulation of laccase and cellulase in relation to fruit body formation in the mycelium of Lentinula edodes on a sawdust-based substrate. Mycoscience 4:149–153
Ohm RA, de Jong JF, de Bekker C, Wosten HA, Lugones LG (2011) Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation. Mol Microbiol 81:1433–1445
Ohm RA, de Jong JF, Lugones LG et al (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28:957–1110
Osipov EM, Polyakov KM, Tikhonova TV et al (2014) Structural and kinetic characterization of a chloride resistant laccase from botrytis aclada. NCBI, Molecular modeling database. http://www.ncbi.nlm.nih.gov/Structure/mmdb/mmdbsrv.cgi?uid=3sqr. Accessed 12 June 2014
Palmer GE, Horton JS (2006) Mushrooms by magic: making connections between signal transductionand fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiol Lett 262:1–8
Pezzella C, Lettera V, Piscitelli A, Giardina P, Sannia G (2013) Transcriptional analysis of Pleurotus ostreatus laccase genes. Appl Microbiol Biotechnol 97:705–717
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007
Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-A resolution containing a full complement of coppers. J Biol Chem 277:37663–37669
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
Quintanar L, Stoj C, Taylor AB, Hart PJ, Kosman DJ, Solomon EI (2007) Shall we dance? How a multicopper oxidase chooses its electron transfer partner. Acc Chem Res 40:445–452
Raper J (1966) Sexuality of higher fungi. The Roland Press, New York
Raper JR, Hoffman RM (1974) Schizophyllum commune. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 597–626
Rodriguez Couto S, Toca Herrera JL (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24:500–513
Rushmore TH, King RG, Paulson KE, Pickett CB (1990) Regulation of glutathione S-transferase Ya subunit gene expression: Identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. PNAS 87:3826–3830
Rushmore TH, Morton MR, Pickett CB (1991) The Antioxidant Responsive Element: Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 266:11632–11639
Sakurai T, Kataoka K (2007) Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 7:220–229
Sanchez C, Tellez-Tellez M, Diaz-Godinez G, Moore D (2004) Simple staining detects ultrastructural and biochemical differentiation of vegetative hyphae and fruit body initials in colonies of Pleurotus pulmonarius. Lett Appl Microbiol 38:483–487
Sharma KK, Kuhad RC (2008) Laccase: enzyme revisited and function redefined. Indian J Microbiol 48:309–316
Solomon EI, Sundaram UM, Machonkin T (1996) Multicopper Oxidases and Oxygenases. Chem Rev 96:2563–2606
Stamatakis A, Hoover P, Rougemont J (2008) A Rapid Bootstrap Algorithm for the RAxML Web-Servers. Syst Biol 75:758–771
Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32:169–178
Strong PJ, Claus H (2011) Laccase: A Review of Its Past and Its Future in Bioremediation. Crit Rev Environ Sci Technol 41:373–434
Taylor AB, Stoj CS, Ziegler L, Kosman DJ, Hart PJ (2005) The copper-iron connection in biology: Structure of the metallo-oxidase Fet3p. PNAS 102:15459–15464
Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:18
Worrall JJ, Chet I, Hüttermann A (1986) Association of Rhizomorph Formation with Laccase Activity in Armillaria spp. J Gen Microbiol 132:2527–2533
Xu LJ, Wang HX, Ng TB (2012) A laccase with HIV-1 reverse transcriptase inhibitory activity from the broth of mycelial culture of the mushroom Lentinus tigrinus. J Biomed Biotechnol. doi:10.1155/2012/536725
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform 9:40
Zhao J, Kwan HS (1999) Characterization, molecular cloning and differential expression analysis of laccasse genes from edible mushroom Lentinula edodes. Appl Environ Microbiol 65:4908–4913
Acknowledgments
We would like to thank DFG GRK-1257 and the Jena School for Microbial Communication (JSMC) for financial support. We thank Manu Singh and Imam Hardiman for their support.
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Madhavan, S., Krause, K., Jung, EM. et al. Differential regulation of multi-copper oxidases in Schizophyllum commune during sexual development. Mycol Progress 13, 1009 (2014). https://doi.org/10.1007/s11557-014-1009-8
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DOI: https://doi.org/10.1007/s11557-014-1009-8