Induction of antibacterial proteins and peptides in the coprophilous mushroom Coprinopsis cinerea in response to bacteria.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
03 2019
03 2019
Historique:
received:
12
01
2018
accepted:
25
09
2018
revised:
23
08
2018
pubmed:
12
10
2018
medline:
15
8
2019
entrez:
11
10
2018
Statut:
ppublish
Résumé
Bacteria are the main nutritional competitors of saprophytic fungi during colonization of their ecological niches. This competition involves the mutual secretion of antimicrobials that kill or inhibit the growth of the competitor. Over the last years it has been demonstrated that fungi respond to the presence of bacteria with changes of their transcriptome, but the significance of these changes with respect to competition for nutrients is not clear as functional proof of the antibacterial activity of the induced gene products is often lacking. Here, we report the genome-wide transcriptional response of the coprophilous mushroom Coprinopsis cinerea to the bacteria Bacillus subtilis and Escherichia coli. The genes induced upon co-cultivation with each bacterium were highly overlapping, suggesting that the fungus uses a similar arsenal of effectors against Gram-positive and -negative bacteria. Intriguingly, the induced genes appeare to encode predominantly secreted peptides and proteins with predicted antibacterial activities, which was validated by comparative proteomics of the C. cinerea secretome. Induced members of two putative antibacterial peptide and protein families in C. cinerea, the cysteine-stabilized αβ-defensins (Csαβ-defensins) and the GH24-type lysozymes, were purified, and their antibacterial activity was confirmed. These results provide compelling evidence that fungi are able to recognize the presence of bacteria and respond with the expression of an arsenal of secreted antibacterial peptides and proteins.
Identifiants
pubmed: 30301946
doi: 10.1038/s41396-018-0293-8
pii: 10.1038/s41396-018-0293-8
pmc: PMC6461984
doi:
Substances chimiques
Anti-Bacterial Agents
0
Defensins
0
Fungal Proteins
0
Peptides
0
Muramidase
EC 3.2.1.17
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Pagination
588-602Références
Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, et al. Bacterial-fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev. 2018;42:335–52.
pubmed: 29471481
Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev. 2011;75:583–609.
pubmed: 22126995
pmcid: 3232736
Moller J, Miller M, Kjoller A. Fungal-bacterial interaction on beech leaves: influence on decomposition and dissolved organic carbon quality. Soil Biol Biochem. 1999;31:367–74.
Rousk J, Baath E. Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol. 2011;78:17–30.
pubmed: 21470255
Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29:795–811.
pubmed: 16102603
Hoffmeister D, Keller NP. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep. 2007;24:393–416.
pubmed: 17390002
Kempken F, Rohlfs M. Fungal secondary metabolite biosynthesis-a chemical defence strategy against antagonistic animals? Fungal Ecol. 2010;3:107–14.
Kunzler M. Hitting the sweet spot-glycans as targets of fungal defense effector proteins. Molecules. 2015;20:8144–67.
pubmed: 25955890
pmcid: 6272156
Macheleidt J, Mattern DJ, Fischer J, Netzker T, Weber J, Schroeckh V, et al. Regulation and role of fungal secondary metabolites. Annu Rev Genet. 2016;50:371–92.
pubmed: 27732794
Adnani N, Rajski SR, Bugni TS. Symbiosis-inspired approaches to antibiotic discovery. Nat Prod Rep. 2017;34:784–814.
pubmed: 28561849
pmcid: 5555300
Netzker T, Fischer J, Weber J, Mattern DJ, Konig CC, Valiante V, et al. Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol. 2015;6:299.
pubmed: 25941517
pmcid: 4403501
Wiemann P, Keller NP. Strategies for mining fungal natural products. J Ind Microbiol Biotechnol. 2014;41:301–13.
pubmed: 24146366
Meldau S, Erb M, Baldwin IT. Defence on demand: mechanisms behind optimal defence patterns. Ann Bot. 2012;110:1503–14.
pubmed: 23022676
pmcid: 3503495
Choi HW, Klessig DF. DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol. 2016;16:232.
pubmed: 27782807
pmcid: 5080799
Essig A, Hofmann D, Munch D, Gayathri S, Kunzler M, Kallio PT, et al. Copsin, a novel peptide-based fungal antibiotic interfering with the peptidoglycan synthesis. J Biol Chem. 2014;289:34953–64.
pubmed: 25342741
pmcid: 4263892
Stockli M, Lin CW, Sieber R, Plaza DF, Ohm RA, Kunzler M. Coprinopsis cinerea intracellular lactonases hydrolyze quorum sensing molecules of Gram-negative bacteria. Fungal Genet Biol. 2017;102:49–62.
pubmed: 27475110
Plaza DF, Lin CW, van der Velden NS, Aebi M, Kunzler M. Comparative transcriptomics of the model mushroom Coprinopsis cinerea reveals tissue-specific armories and a conserved circuitry for sexual development. BMC Genom. 2014;15:492.
Sabotic J, Ohm RA, Kunzler M. Entomotoxic and nematotoxic lectins and protease inhibitors from fungal fruiting bodies. Appl Microbiol Biotechnol. 2016;100:91–111.
pubmed: 26521246
Plaza DF, Schmieder SS, Lipzen A, Lindquist E, Kunzler M. Identification of a novel nematotoxic protein by challenging the model mushroom coprinopsis cinerea with a fungivorous nematode. G3. 2015;6:87–98.
pubmed: 26585824
Bleuler-Martinez S, Butschi A, Garbani M, Walti MA, Wohlschlager T, Potthoff E, et al. A lectin-mediated resistance of higher fungi against predators and parasites. Mol Ecol. 2011;20:3056–70.
pubmed: 21486374
Doll K, Chatterjee S, Scheu S, Karlovsky P, Rohlfs M. Fungal metabolic plasticity and sexual development mediate induced resistance to arthropod fungivory. Proc Biol Sci. 2013;280:20131219.
pubmed: 24068353
pmcid: 3790476
Rohlfs M, Albert M, Keller NP, Kempken F. Secondary chemicals protect mould from fungivory. Biol Lett. 2007;3:523–5.
pubmed: 17686752
pmcid: 2391202
Deveau A, Barret M, Diedhiou AG, Leveau J, de Boer W, Martin F, et al. Pairwise transcriptomic analysis of the interactions between the ectomycorrhizal fungus Laccaria bicolor S238N and three beneficial, neutral and antagonistic soil bacteria. Microb Ecol. 2015;69:146–59.
pubmed: 25085516
Gkarmiri K, Finlay RD, Alstrom S, Thomas E, Cubeta MA, Hogberg N. Transcriptomic changes in the plant pathogenic fungus Rhizoctonia solani AG-3 in response to the antagonistic bacteria Serratia proteamaculans and Serratia plymuthica. BMC Genom. 2015;16:630.
Ipcho S, Sundelin T, Erbs G, Kistler HC, Newman MA, Olsson S. Fungal innate immunity induced by bacterial Microbe-Associated Molecular Patterns (MAMPs). G3. 2016;6:1585–95.
pubmed: 27172188
Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M. Overlapping podospora anserina transcriptional responses to bacterial and fungal non self indicate a multilayered innate immune response. Front Microbiol. 2016;7:471.
pubmed: 27148175
pmcid: 4835503
Mathioni SM, Patel N, Riddick B, Sweigard JA, Czymmek KJ, Caplan JL, et al. Transcriptomics of the rice blast fungus Magnaporthe oryzae in response to the bacterial antagonist Lysobacter enzymogenes reveals candidate fungal defense response genes. PLoS ONE. 2013;8:e76487.
pubmed: 24098512
pmcid: 3789685
Mela F, Fritsche K, de Boer W, van Veen JA, de Graaff LH, van den Berg M, et al. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J. 2011;5:1494–504.
pubmed: 21614084
pmcid: 3160687
Benoit I, van den Esker MH, Patyshakuliyeva A, Mattern DJ, Blei F, Zhou M, et al. Bacillus subtilis attachment to Aspergillus niger hyphae results in mutually altered metabolism. Environ Microbiol. 2015;17:2099–113.
pubmed: 25040940
Schroeckh V, Scherlach K, Nutzmann HW, Shelest E, Schmidt-Heck W, Schuemann J, et al. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA. 2009;106:14558–63.
pubmed: 19666480
Oh DC, Kauffman CA, Jensen PR, Fenical W. Induced production of emericellamides A and B from the marine-derived fungus Emericella sp. in competing co-culture. J Nat Prod. 2007;70:515–20.
pubmed: 17323993
Ola AR, Thomy D, Lai D, Brotz-Oesterhelt H, Proksch P. Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod. 2013;76:2094–9.
pubmed: 24175613
Wohlkonig A, Huet J, Looze Y, Wintjens R. Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs. PLoS ONE. 2010;5:e15388.
pubmed: 21085702
pmcid: 2976769
Swamy S, Uno I, Ishikawa T. Morphogenetic effects of mutations at the a and B incompatibility factors in Coprinus-Cinereus. J Gen Microbiol. 1984;130:3219–24.
Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis. P Natl Acad Sci USA. 2001;98:11621–6.
Hatakeyama M, Opitz L, Russo G, Qi W, Schlapbach R, Rehrauer H. SUSHI: an exquisite recipe for fully documented, reproducible and reusable NGS data analysis. BMC Bioinforma. 2016;17:228.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
Muraguchi H, Umezawa K, Niikura M, Yoshida M, Kozaki T, Ishii K, et al. Strand-Specific RNA-Seq Analyses of Fruiting Body Development in Coprinopsis cinerea. PLoS ONE. 2015;10:e0141586.
pubmed: 26510163
pmcid: 4624876
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–30.
pubmed: 24227677
pmcid: 24227677
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
pubmed: 25516281
pmcid: 25516281
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–6.
pubmed: 25414356
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.
pubmed: 10802651
pmcid: 3037419
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–6.
pubmed: 21221095
pmcid: 3346182
Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–6.
pubmed: 21959131
Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–80.
pubmed: 11152613
Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. 2002;00:2.3.1–2.3.22.
Franzoi M, van Heuvel Y, Thomann S, Schurch N, Kallio PT, Venier P, et al. Structural Insights into the mode of action of the peptide antibiotic copsin. Biochemistry. 2017;56:4992–5001.
pubmed: 28825809
Wu S, Letchworth GJ. High efficiency transformation by electroporation of Pichia pastoris pretreated with lithium acetate and dithiothreitol. Biotechniques. 2004;36:152–4.
pubmed: 14740498
Meskauskas A, Novak Frazer L, Moore D. Mathematical modelling of morphogenesis in fungi: a key role for curvature compensation (‘autotropism’) in the local curvature distribution model. New Phytol. 1999;143:387–99.
pubmed: 11542911
Kunst, F. et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249–256 (1997)
Droce A, Sorensen JL, Giese H, Sondergaard TE. Glass bead cultivation of fungi: combining the best of liquid and agar media. J Microbiol Methods. 2013;94:343–6.
pubmed: 23871859
Brandenburger E, Braga D, Kombrink A, Lackner G, Gressler J, Kunzler M, et al. Multi-genome analysis identifies functional and phylogenetic diversity of basidiomycete adenylate-forming reductases. Fungal Genet Biol. 2016;112:55–63.
pubmed: 27457378
Agger S, Lopez-Gallego F, Schmidt-Dannert C. Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Mol Microbiol. 2009;72:1181–95.
pubmed: 19400802
pmcid: 2723806
Stajich JE, Wilke SK, Ahren D, Au CH, Birren BW, Borodovsky M, et al. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci USA. 2010;107:11889–94.
pubmed: 20547848
Coleman JJ, Mylonakis E. Efflux in fungi: la piece de resistance. PLoS Pathog. 2009;5:e1000486.
pubmed: 19557154
pmcid: 2695561
Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, et al. Fungal effectors and plant susceptibility. Annu Rev Plant Biol. 2015;66:513–45.
pubmed: 25923844
Plett JM, Daguerre Y, Wittulsky S, Vayssieres A, Deveau A, Melton SJ, et al. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci USA. 2014;111:8299–304.
pubmed: 24847068
Sanchez-Vallet A, Mesters JR, Thomma BP. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol Rev. 2015;39:171–83.
pubmed: 25725011
Baldrian P. Fungal laccases-occurrence and properties. FEMS Microbiol Rev. 2006;30:215–42.
pubmed: 16472305
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10:845–58.
pubmed: 25950237
pmcid: 5298202
Mygind PH, Fischer RL, Schnorr KM, Hansen MT, Sonksen CP, Ludvigsen S, et al. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature. 2005;437:975–80.
pubmed: 16222292
Zhu S. Discovery of six families of fungal defensin-like peptides provides insights into origin and evolution of the CSalphabeta defensins. Mol Immunol. 2008;45:828–38.
pubmed: 17675235
Weaver LH, Matthews BW. Structure of bacteriophage T4 lysozyme refined at 1.7 A resolution. J Mol Biol. 1987;193:189–99.
pubmed: 3586019
Young R. Bacteriophage lysis: mechanism and regulation. Microbiol Rev. 1992;56:430–81.
pubmed: 1406491
pmcid: 372879
Kuroki R, Weaver LH, Matthews BW. A covalent enzyme-substrate intermediate with saccharide distortion in a mutant T4 lysozyme. Science. 1993;262:2030–3.
pubmed: 8266098
Selsted ME, Martinez RJ. A simple and ultrasensitive enzymatic assay for the quantitative determination of lysozyme in the picogram range. Anal Biochem. 1980;109:67–70.
pubmed: 7469020
Bera A, Herbert S, Jakob A, Vollmer W, Gotz F. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol. 2005;55:778–87.
pubmed: 15661003
Jones JD, Dangl JL. The plant immune system. Nature. 2006;444:323–9.
pubmed: 17108957
pmcid: 17108957
Rovenich H, Boshoven JC, Thomma BP. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr Opin Plant Biol. 2014;20:96–103.
pubmed: 24879450
Zeilinger S, Gupta VK, Dahms TE, Silva RN, Singh HB, Upadhyay RS, et al. Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev. 2016;40:182–207.
pubmed: 26591004
Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA. 2011;108:9166–71.
pubmed: 21536894
Powell AJ, Conant GC, Brown DE, Carbone I, Dean RA. Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genom. 2008;9:147.
Martin JF, Liras P. Evolutionary formation of gene clusters by reorganization: the meleagrin/roquefortine paradigm in different fungi. Appl Microbiol Biotechnol. 2016;100:1579–87.
pubmed: 26668029
Hurst LD, Pal C, Lercher MJ. The evolutionary dynamics of eukaryotic gene order. Nat Rev Genet. 2004;5:299–310.
pubmed: 15131653
Batada NN, Urrutia AO, Hurst LD. Chromatin remodelling is a major source of coexpression of linked genes in yeast. Trends Genet. 2007;23:480–4.
pubmed: 17822800
Oeemig JS, Lynggaard C, Knudsen DH, Hansen FT, Norgaard KD, Schneider T, et al. Eurocin, a new fungal defensin: structure, lipid binding, and its mode of actioN. J Biol Chem. 2012;287:42361–72.
pubmed: 23093408
pmcid: 3516779
Wu J, Liu S, Wang H. Invasive fungi-derived defensins kill drug-resistant bacterial pathogens. Peptides. 2018;99:82–91.
pubmed: 29174563
Wu Y, Gao B, Zhu S. New fungal defensin-like peptides provide evidence for fold change of proteins in evolution. Biosci Rep. 2017;37:BSR20160438.
Schmelcher M, Waldherr F, Loessner MJ. Listeria bacteriophage peptidoglycan hydrolases feature high thermoresistance and reveal increased activity after divalent metal cation substitution. Appl Microbiol Biotechnol. 2012;93:633–43.
pubmed: 21720825
Xu XL, Lee RT, Fang HM, Wang YM, Li R, Zou H, et al. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe. 2008;4:28–39.
pubmed: 18621008
Bertsche U, Mayer C, Gotz F, Gust AA. Peptidoglycan perception-sensing bacteria by their common envelope structure. Int J Med Microbiol. 2015;305:217–23.
pubmed: 25596887
Uehling J, Deveau A, Paoletti M. Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems. PLoS Pathog. 2017;13:e1006578.
pubmed: 29073287
pmcid: 5658179
Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42:D699–704.
pubmed: 24297253