Specialisation events of fungal metacommunities exposed to a persistent organic pollutant are suggestive of augmented pathogenic potential
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
647928
European Research Council - International
PubMed
30466483
PubMed Central
PMC6251201
DOI
10.1186/s40168-018-0589-y
PII: 10.1186/s40168-018-0589-y
Knihovny.cz E-zdroje
- MeSH
- dusík metabolismus MeSH
- houby účinky léků genetika metabolismus MeSH
- látky znečišťující životní prostředí toxicita MeSH
- lesy MeSH
- mikrobiota účinky léků MeSH
- pentachlorfenol toxicita MeSH
- proteom genetika MeSH
- spory hub růst a vývoj MeSH
- uhlík metabolismus MeSH
- znečištění životního prostředí analýza MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- dusík MeSH
- látky znečišťující životní prostředí MeSH
- pentachlorfenol MeSH
- proteom MeSH
- uhlík MeSH
BACKGROUND: The impacts of man-made chemicals, in particular of persistent organic pollutants, are multifactorial as they may affect the integrity of ecosystems, alter biodiversity and have undesirable effects on many organisms. We have previously demonstrated that the belowground mycobiota of forest soils acts as a buffer against the biocide pollutant pentachlorophenol. However, the trade-offs made by mycobiota to mitigate this pollutant remain cryptic. RESULTS: Herein, we demonstrate using a culture-dependent approach that exposure to pentachlorophenol led to alterations in the composition and functioning of the metacommunity, many of which were not fully alleviated when most of the biocide was degraded. Proteomic and physiological analyses showed that the carbon and nitrogen metabolisms were particularly affected. This dysregulation is possibly linked to the higher pathogenic potential of the metacommunity following exposure to the biocide, supported by the secretion of proteins related to pathogenicity and reduced susceptibility to a fungicide. Our findings provide additional evidence for the silent risks of environmental pollution, particularly as it may favour the development of pathogenic trade-offs in fungi, which may impose serious threats to animals and plant hosts.
Instituto Nacional Investigação Agrária e Veterinária Av da República 2780 157 Oeiras Portugal
Serra Hunter Fellow Generalitat de Catalunya Barcelona Spain
Zobrazit více v PubMed
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59–67. doi: 10.1038/nature11148. PubMed DOI
Backhaus T, Snape J, Lazorchak J. The impact of chemical pollution on biodiversity and ecosystem services: the need for an improved understanding. Integr Environ Assess Manag. 2012;8:575–576. doi: 10.1002/ieam.1353. PubMed DOI
Naeem S, Duffy JE, Zavaleta E. The functions of biological diversity in an age of extinction. Science. 2012;336:1401–1406. doi: 10.1126/science.1215855. PubMed DOI
Varela A, Martins C, Silva Pereira C. A three-act play: pentachlorophenol threats to the cork oak forest soils mycobiome. Curr Opin Microbiol. 2017;37:142–149. doi: 10.1016/j.mib.2017.06.007. PubMed DOI
Czaplicka M. Sources and transformations of chlorophenols in the natural environment. Sci Total Environ. 2004;322:21–39. doi: 10.1016/j.scitotenv.2003.09.015. PubMed DOI
Morgan M, Jones P, Sobus J. Short-term variability and predictors of urinary pentachlorophenol levels in Ohio preschool children. Int J Environ Res Public Health. 2015;12:800–815. doi: 10.3390/ijerph120100800. PubMed DOI PMC
Varela A, Martins C, Núñez O, Martins I, Houbraken JA, Martins TM, Leitão MC, McLellan I, Vetter W, Galceran MT, Silva Pereira C. Understanding fungal functional biodiversity during the mitigation of environmentally dispersed pentachlorophenol in cork oak forest soils. Environ Microbiol. 2015;17:2922–2934. doi: 10.1111/1462-2920.12837. PubMed DOI
Harms H, Schlosser D, Wick LY. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol. 2011;9:177–192. doi: 10.1038/nrmicro2519. PubMed DOI
Carvalho MB, Martins I, Medeiros J, Tavares S, Planchon S, Renaut J, Nunez O, Gallart-Ayala H, Galceran MT, Hursthouse A, Silva Pereira C. The response of Mucor plumbeus to pentachlorophenol: a toxicoproteomics study. J Proteome. 2013;78:159–171. doi: 10.1016/j.jprot.2012.11.006. PubMed DOI
Carvalho MB, Tavares S, Medeiros J, Núñez O, Gallart-Ayalla H, Leitão MC, Galceran MT, Hursthouse A, Silva Pereira C. Degradation pathway of pentachlorophenol by Mucor plumbeus involves phase II conjugation and oxidation-reduction reactions. J Hazard Mater. 2011;198:133–142. doi: 10.1016/j.jhazmat.2011.10.021. PubMed DOI
Gadd GM. Fungi in bioremediation: Cambridge University Press; 2001.
Martins TM, Nunez O, Gallart-Ayala H, Leitao MC, Galceran MT, Silva Pereira C. New branches in the degradation pathway of monochlorocatechols by Aspergillus nidulans: a metabolomics analysis. J Hazard Mater. 2014;268:264–272. doi: 10.1016/j.jhazmat.2014.01.024. PubMed DOI
Větrovský Tomáš, Baldrian Petr, Morais Daniel. SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics. 2018;34(13):2292–2294. doi: 10.1093/bioinformatics/bty071. PubMed DOI PMC
Žifčáková L, Větrovský T, Howe A, Baldrian P. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol. 2016;18:288–301. doi: 10.1111/1462-2920.13026. PubMed DOI
Morel G, Sterck L, Swennen D, Marcet-Houben M, Onesime D, Levasseur A, Jacques N, Mallet S, Couloux A, Labadie K, et al. Differential gene retention as an evolutionary mechanism to generate biodiversity and adaptation in yeasts. Sci Rep. 2015;5:11571. doi: 10.1038/srep11571. PubMed DOI PMC
Fuchs G, Boll M, Heider J. Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol. 2011;9:803. doi: 10.1038/nrmicro2652. PubMed DOI
Medina-Silva R, Barros MP, Galhardo RS, Netto LE, Colepicolo P, Menck CF. Heat stress promotes mitochondrial instability and oxidative responses in yeast deficient in thiazole biosynthesis. Res Microbiol. 2006;157:275–281. doi: 10.1016/j.resmic.2005.07.004. PubMed DOI
Limjindaporn T, Khalaf RA, Fonzi WA. Nitrogen metabolism and virulence of Candida albicans require the GATA-type transcriptional activator encoded by GAT1. Mol Microbiol. 2003;50:993–1004. doi: 10.1046/j.1365-2958.2003.03747.x. PubMed DOI
Bolton MD, Thomma BP. The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiol Mol Plant Pathol. 2008;72:104–110. doi: 10.1016/j.pmpp.2008.07.001. DOI
Seidler NW. In GAPDH: Biological Properties and Diversity Springer. 2013. GAPDH, as a virulence factor; pp. 149–178. PubMed
Dubovenko AG, Dunaevsky YE, Belozersky MA, Oppert B, Lord JC, Elpidina EN. Trypsin-like proteins of the fungi as possible markers of pathogenicity. Fungal Biol. 2010;114:151–159. doi: 10.1016/j.funbio.2009.11.004. PubMed DOI
Mir AA, Park S-Y, Sadat MA, Kim S, Choi J, Jeon J, Lee Y-H. Systematic characterization of the peroxidase gene family provides new insights into fungal pathogenicity in Magnaporthe oryzae. Sci Rep. 2015;5:11831. doi: 10.1038/srep11831. PubMed DOI PMC
Selvam RM, Nithya R, Devi PN, Shree RSB, Nila MV, Demonte NL, Thangavel C, Maheshwari JJ, Lalitha P, Prajna NV, Dharmalingam K. Exoproteome of Aspergillus flavus corneal isolates and saprophytes: identification of proteoforms of an oversecreted alkaline protease. J Proteome. 2015;115:23–35. doi: 10.1016/j.jprot.2014.11.017. PubMed DOI
Huang Z, Hao Y, Gao T, Huang Y, Ren S, Keyhani NO. The Ifchit1 chitinase gene acts as a critical virulence factor in the insect pathogenic fungus Isaria fumosorosea. Appl Microbiol Biotechnol. 2016;100:5491–5503. doi: 10.1007/s00253-016-7308-z. PubMed DOI
Garfoot AL, Dearing KL, VanSchoiack AD, Wysocki VH, Rappleye CA. Eng1 and Exg8 are the major β-glucanases secreted by the fungal pathogen Histoplasma capsulatum. J Biol Chem. 2017;292:4801–4810. doi: 10.1074/jbc.M116.762104. PubMed DOI PMC
Davis DA. How human pathogenic fungi sense and adapt to pH: the link to virulence. Curr Opin Microbiol. 2009;12:365–370. doi: 10.1016/j.mib.2009.05.006. PubMed DOI
Fairlamb AH, Gow NA, Matthews KR, Waters AP. Drug resistance in eukaryotic microorganisms. Nat Microbiol. 2016;1:16092. doi: 10.1038/nmicrobiol.2016.92. PubMed DOI PMC
Denning DW, Bromley MJ. How to bolster the antifungal pipeline. Science. 2015;347:1414–1416. doi: 10.1126/science.aaa6097. PubMed DOI
Low-Décarie E, Kolber M, Homme P, Lofano A, Dumbrell A, Gonzalez A, Bell G. Community rescue in experimental metacommunities. Proc Natl Acad Sci U S A. 2015;112:14307–14312. doi: 10.1073/pnas.1513125112. PubMed DOI PMC
Martins I, Garcia H, Varela A, Núñez O, Planchon S, Galceran MT, Renaut J, Rebelo LP, Silva Pereira C. Investigating Aspergillus nidulans secretome during colonisation of cork cell walls. J Proteome. 2014;98:175–188. doi: 10.1016/j.jprot.2013.11.023. PubMed DOI
Liu B, Tu C, Hu S, Gumpertz M, Ristaino JB. Effect of organic, sustainable, and conventional management strategies in grower fields on soil physical, chemical, and biological factors and the incidence of southern blight. Appl Soil Ecol. 2007;37:202–214. doi: 10.1016/j.apsoil.2007.06.007. DOI
Preston-Mafham J, Boddy L, Randerson PF. Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles–a critique. FEMS Microbiol Ecol. 2002;42:1–14. PubMed
Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, Murrell JC. DNA stable-isotope probing. Nat Protoc. 2007;2:860. doi: 10.1038/nprot.2007.109. PubMed DOI
Ihrmark K, Bödeker I, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE. New primers to amplify the fungal ITS2 region–evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol. 2012;82:666–677. doi: 10.1111/j.1574-6941.2012.01437.x. PubMed DOI
Aronesty Erik. Comparison of Sequencing Utility Programs. The Open Bioinformatics Journal. 2013;7(1):1–8. doi: 10.2174/1875036201307010001. DOI
Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Kristiansson E, Ryberg M, Jumpponen A, Abarenkov K. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol. 2010;3:284–287. doi: 10.1016/j.funeco.2010.05.002. DOI
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996. doi: 10.1038/nmeth.2604. PubMed DOI
Méchin V, Damerval C, Zivy M. Total protein extraction with TCA-acetone. In: Thiellement H, Zivy M, Damerval C, Méchin V, editors. Plant proteomics. Totowa: Springer; 2007. p. 1–8. PubMed
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP. Statistical analysis of membrane proteome expression changes in Saccharomyces c erevisiae. J Proteome Res. 2006;5:2339–2347. doi: 10.1021/pr060161n. PubMed DOI
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC
Kammers K, Cole RN, Tiengwe C, Ruczinski I. Detecting significant changes in protein abundance. EuPA Open Proteomics. 2015;7:11–19. doi: 10.1016/j.euprot.2015.02.002. PubMed DOI PMC
Gatto L, Breckels LM, Naake T, Gibb S. Visualization of proteomics data using R and bioconductor. Proteomics. 2015;15:1375–1389. doi: 10.1002/pmic.201400392. PubMed DOI PMC
Vizcaíno JA, Csordas A, Del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 2015;44:D447–D456. doi: 10.1093/nar/gkv1145. PubMed DOI PMC