1887

Abstract

Production of basidiomycete atromentin-derived pigments like variegatic acid (pulvinic acid-type) and involutin (diarylcyclopentenone) from the brown-rotter Serpula lacrymans and the ectomycorrhiza-forming Paxillus involutus, respectively, is induced by complex nutrition, and in the case of S. lacrymans, bacteria. Pigmentation in S. lacrymans was stimulated by 13 different bacteria and cell-wall-damaging enzymes (lytic enzymes and proteases), but not by lysozyme or mechanical damage. The use of protease inhibitors with Bacillus subtilis or heat-killed bacteria during co-culturing with S. lacrymans significantly reduced pigmentation indicating that enzymatic hyphal damage and/or released peptides, rather than mechanical injury, was the major cause of systemic pigment induction. Conversely, no significant pigmentation by bacteria was observed from P. involutus. We found additional putative transcriptional composite elements of atromentin synthetase genes in P. involutus and other ectomycorrhiza-forming species that were absent from S. lacrymans and other brown-rotters. Variegatic and its precursor xerocomic acid, but not involutin, in return inhibited swarming and colony biofilm spreading of Bacillus subtilis, but did not kill B. subtilis. We suggest that dissimilar pigment regulation by fungal lifestyle was a consequence of pigment bioactivity and additional promoter motifs. The focus on basidiomycete natural product gene induction and regulation will assist in future studies to determine global regulators, signalling pathways and associated transcription factors of basidiomycetes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000582
2017-12-05
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/1/65.html?itemId=/content/journal/micro/10.1099/mic.0.000582&mimeType=html&fmt=ahah

References

  1. Gill M, Steglich W. Pigments of fungi (Macromycetes). Prog Chem Org Nat Prod 1987;51:1–317
    [Google Scholar]
  2. Wackler B, Lackner G, Chooi YH, Hoffmeister D. Characterization of the Suillus grevillei quinone synthetase GreA supports a nonribosomal code for aromatic α-keto acids. Chembiochem 2012;13:1798–1804 [CrossRef][PubMed]
    [Google Scholar]
  3. Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P et al. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 2011;333:762–765 [CrossRef][PubMed]
    [Google Scholar]
  4. Shah F, Schwenk D, Nicolás C, Persson P, Hoffmeister D et al. Involutin is an Fe3+ reductant secreted by the ectomycorrhizal fungus Paxillus involutus during Fenton-based decomposition of organic matter. Appl Environ Microbiol 2015;81:8427–8433 [CrossRef][PubMed]
    [Google Scholar]
  5. Kauserud H, Svegården IB, Saetre GP, Knudsen H, Stensrud Ø et al. Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans. Mol Ecol 2007;16:3350–3360 [CrossRef][PubMed]
    [Google Scholar]
  6. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 2015;47:410–415 [CrossRef][PubMed]
    [Google Scholar]
  7. Pellitier PT, Zak DR. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytol 2017; doi: 10.1111/nph.14598 [CrossRef]
    [Google Scholar]
  8. Braesel J, Götze S, Shah F, Heine D, Tauber J et al. Three redundant synthetases secure redox-active pigment production in the basidiomycete Paxillus involutus. Chem Biol 2015;22:1325–1334 [CrossRef][PubMed]
    [Google Scholar]
  9. Tauber JP, Schroeckh V, Shelest E, Brakhage AA, Hoffmeister D. Bacteria induce pigment formation in the basidiomycete Serpula lacrymans. Environ Microbiol 2016;18:5218–5227 [CrossRef][PubMed]
    [Google Scholar]
  10. Schneider P, Bouhired S, Hoffmeister D. Characterization of the atromentin biosynthesis genes and enzymes in the homobasidiomycete Tapinella panuoides. Fungal Genet Biol 2008;45:1487–1496 [CrossRef][PubMed]
    [Google Scholar]
  11. Wawrzyn GT, Quin MB, Choudhary S, López-Gallego F, Schmidt-Dannert C. Draft genome of Omphalotus olearius provides a predictive framework for sesquiterpenoid natural product biosynthesis in Basidiomycota. Chem Biol 2012;19:772–783 [CrossRef][PubMed]
    [Google Scholar]
  12. Rineau F, Roth D, Shah F, Smits M, Johansson T et al. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ Microbiol 2012;14:1477–1487 [CrossRef][PubMed]
    [Google Scholar]
  13. van Schöll L, Hoffland E, van Breemen N. Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol 2006;170:153–163 [CrossRef][PubMed]
    [Google Scholar]
  14. Essig A, Hofmann D, Münch D, Gayathri S, Künzler M et al. Copsin, a novel peptide-based fungal antibiotic interfering with the peptidoglycan synthesis. J Biol Chem 2014;289:34953–34964 [CrossRef][PubMed]
    [Google Scholar]
  15. Turner S, Pryer KM, Miao VP, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 1999;46:327–338 [CrossRef][PubMed]
    [Google Scholar]
  16. Lane DJ. 16S/23S rRNA Sequencing New York, NY: John Wiley and Sons; 1991
    [Google Scholar]
  17. Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 2014;42:D699–D704 [CrossRef][PubMed]
    [Google Scholar]
  18. Branco S, Gladieux P, Ellison CE, Kuo A, Labutti K et al. Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol Ecol 2015;24:2747–2758 [CrossRef][PubMed]
    [Google Scholar]
  19. Floudas D, Binder M, Riley R, Barry K, Blanchette RA et al. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 2012;336:1715–1719 [CrossRef][PubMed]
    [Google Scholar]
  20. Wolf T, Shelest V, Nath N, Shelest E. CASSIS and SMIPS: promoter-based prediction of secondary metabolite gene clusters in eukaryotic genomes. Bioinformatics 2016;32:1138–1143 [CrossRef][PubMed]
    [Google Scholar]
  21. Bailey TL, Boden M, Buske FA, Frith M, Grant CE et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009;37:W202–W208 [CrossRef][PubMed]
    [Google Scholar]
  22. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 1994;2:28–36[PubMed]
    [Google Scholar]
  23. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  24. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008;36:W465–W469 [CrossRef][PubMed]
    [Google Scholar]
  25. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010;59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  26. Lefort V, Longueville JE, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol 2017;34:2422–2424 [CrossRef][PubMed]
    [Google Scholar]
  27. Griebel T, Brinkmeyer M, Böcker S. EPoS: a modular software framework for phylogenetic analysis. Bioinformatics 2008;24:2399–2400 [CrossRef][PubMed]
    [Google Scholar]
  28. Gallegos-Monterrosa R, Kankel S, Götze S, Barnett R, Stallforth P et al. Lysinibacillus fusiformis M5 Induces Increased Complexity in Bacillus subtilis 168 Colony Biofilms via Hypoxanthine. J Bacteriol 2017;199:e00204-17 [CrossRef][PubMed]
    [Google Scholar]
  29. Hölscher T, Dragoš A, Gallegos-Monterrosa R, Martin M, Mhatre E et al. Monitoring spatial segregation in surface colonizing microbial populations. J Vis Exp 2016;116: doi:10.3791/54752 [CrossRef][PubMed]
    [Google Scholar]
  30. Karigar CS, Rao SS. Role of microbial enzymes in the bioremediation of pollutants: a review. Enzyme Res 2011;2011:1–11 [CrossRef][PubMed]
    [Google Scholar]
  31. Mäntsälä P, Zalkin H. Extracellular and membrane-bound proteases from Bacillus subtilis. J Bacteriol 1980;141:493–501[PubMed]
    [Google Scholar]
  32. Schwenk D, Nett M, Dahse HM, Horn U, Blanchette RA et al. Injury-induced biosynthesis of methyl-branched polyene pigments in a white-rotting basidiomycete. J Nat Prod 2014;77:2658–2663 [CrossRef][PubMed]
    [Google Scholar]
  33. Gruber S, Seidl-Seiboth V. Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 2012;158:26–34 [CrossRef][PubMed]
    [Google Scholar]
  34. Connelly MB, Young GM, Sloma A. Extracellular proteolytic activity plays a central role in swarming motility in Bacillus subtilis. J Bacteriol 2004;186:4159–4167 [CrossRef][PubMed]
    [Google Scholar]
  35. Krishnappa L, Dreisbach A, Otto A, Goosens VJ, Cranenburgh RM et al. Extracytoplasmic proteases determining the cleavage and release of secreted proteins, lipoproteins, and membrane proteins in Bacillus subtilis. J Proteome Res 2013;12:4101–4110 [CrossRef][PubMed]
    [Google Scholar]
  36. Westers L, Westers H, Zanen G, Antelmann H, Hecker M et al. Genetic or chemical protease inhibition causes significant changes in the Bacillus subtilis exoproteome. Proteomics 2008;8:2704–2713 [CrossRef][PubMed]
    [Google Scholar]
  37. Benoit I, van den Esker MH, Patyshakuliyeva A, Mattern DJ, Blei F et al. Bacillus subtilis attachment to Aspergillus niger hyphae results in mutually altered metabolism. Environ Microbiol 2015;17:2099–2113 [CrossRef][PubMed]
    [Google Scholar]
  38. Netzker T, Fischer J, Weber J, Mattern DJ, König CC et al. Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol 2015;6:299 [CrossRef][PubMed]
    [Google Scholar]
  39. Shah F, Nicolás C, Bentzer J, Ellström M, Smits M et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 2016;209:1705–1719 [CrossRef][PubMed]
    [Google Scholar]
  40. de Carvalho MP, Türck P, Abraham WR. Secondary metabolites control the associated bacterial communities of saprophytic basidiomycotina fungi. Microbes Environ 2015;30:196–198 [CrossRef][PubMed]
    [Google Scholar]
  41. Guennoc CM, Rose C, Labbe J, Deveau A. Bacterial biofilm formation on soil fungi: a widespread ability under controls. bioRxiv 2017;130740
    [Google Scholar]
  42. Pent M, Põldmaa K, Bahram M. Bacterial communities in boreal forest mushrooms are shaped both by soil parameters and host identity. Front Microbiol 2017;8:836 [CrossRef][PubMed]
    [Google Scholar]
  43. Bontemps C, Toussaint M, Revol PV, Hotel L, Jeanbille M et al. Taxonomic and functional diversity of Streptomyces in a forest soil. FEMS Microbiol Lett 2013;342:157–167 [CrossRef][PubMed]
    [Google Scholar]
  44. Schrey SD, Erkenbrack E, Früh E, Fengler S, Hommel K et al. Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza-associated streptomycetes. BMC Microbiol 2012;12:164 [CrossRef][PubMed]
    [Google Scholar]
  45. Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 2005;168:205–216 [CrossRef][PubMed]
    [Google Scholar]
  46. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M et al. Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 2006;72:3550–3557 [CrossRef][PubMed]
    [Google Scholar]
  47. Duchesne LUCC, Peterson RL, Ellis BE. Pine root exudate stimulates the synthesis of antifungal compounds by the ectomycorrhizal fungus Paxillus involutus. New Phytol 1988;108:471–476 [CrossRef]
    [Google Scholar]
  48. Voisard C, Wang J, Mcevoy JL, Xu P, Leong SA. urbs1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol Cell Biol 1993;13:7091–7100 [CrossRef][PubMed]
    [Google Scholar]
  49. Shelest E. Transcription Factors in Fungi: TFome Dynamics, Three Major Families, and Dual-Specificity TFs. Front Genet 2017;8:53 [CrossRef][PubMed]
    [Google Scholar]
  50. Yin W, Keller NP. Transcriptional regulatory elements in fungal secondary metabolism. J Microbiol 2011;49:329–339 [CrossRef][PubMed]
    [Google Scholar]
  51. Todd RB, Zhou M, Ohm RA, Leeggangers HA, Visser L et al. Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics 2014;15:214 [CrossRef][PubMed]
    [Google Scholar]
  52. Basse CW, Farfsing JW. Promoters and their regulation in Ustilago maydis and other phytopathogenic fungi. FEMS Microbiol Lett 2006;254:208–216 [CrossRef][PubMed]
    [Google Scholar]
  53. Plaza DF, Lin CW, van der Velden NS, Aebi M, Künzler M. Comparative transcriptomics of the model mushroom Coprinopsis cinerea reveals tissue-specific armories and a conserved circuitry for sexual development. BMC Genomics 2014;15:492 [CrossRef][PubMed]
    [Google Scholar]
  54. Bayram O, Braus GH. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 2012;36:1–24 [CrossRef][PubMed]
    [Google Scholar]
  55. Brakhage AA. Regulation of fungal secondary metabolism. Nat Rev Microbiol 2013;11:21–32 [CrossRef][PubMed]
    [Google Scholar]
  56. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 2001;98:11621–11626 [CrossRef][PubMed]
    [Google Scholar]
  57. Tegos G, Stermitz FR, Lomovskaya O, Lewis K. Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob Agents Chemother 2002;46:3133–3141 [CrossRef][PubMed]
    [Google Scholar]
  58. Stöckli M, Lin CW, Sieber R, Plaza DF, Ohm RA et al. Coprinopsis cinerea intracellular lactonases hydrolyze quorum sensing molecules of Gram-negative bacteria. Fungal Genet Biol 2017;102:49–62 [CrossRef][PubMed]
    [Google Scholar]
  59. Wagner K, Gallegos-Monterrosa R, Sammer D, Kovacs AT, Krause K et al. The ectomycorrhizospheric habitat: Norway spruce and Tricholoma vaccinum shape their environment. Submitted for publication
  60. Scherlach K, Lackner G, Graupner K, Pidot S, Bretschneider T et al. Biosynthesis and mass spectrometric imaging of tolaasin, the virulence factor of brown blotch mushroom disease. Chembiochem 2013;14:2439–2443 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000582
Loading
/content/journal/micro/10.1099/mic.0.000582
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error