Fomes fomentarius is a widespread, wood-rotting fungus of temperate, broadleaved forests. Although the fruiting bodies of F. fomentarius persist for multiple years, little is known about its associated microbiome or how these recalcitrant structures are ultimately decomposed. Here we used metagenomics and metatranscriptomics to analyse the microbial community associated with healthy living and decomposing F. fomentarius fruiting bodies to assess the functional potential of the fruiting body-associated microbiome and to determine the main players involved in fruiting body decomposition. F. fomentarius sequences in the metagenomes were replaced by bacterial sequences as the fruiting body decomposed. Most CAZymes expressed in decomposing fruiting bodies targeted components of the fungal cell wall with almost all chitin-targeting sequences, plus a high proportion of beta-glucan-targeting sequences, belonging to Arthropoda. We suggest that decomposing fruiting bodies of F. fomentarius represent a habitat rich in bacteria, while its decomposition is primarily driven by Arthropoda. Decomposing fruiting bodies thus represent a specific habitat supporting both microorganisms and microfauna.

Laboratory of Environmental Microbiology Institute of Microbiology of the Czech Academy of Sciences 142 00 Prague Czechia

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FEMS Microbiol Ecol. 2024 May 14;100(6):fiae077. doi: 10.1093/femsec/fiae077. PubMed

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Aramaki  T, Blanc-Mathieu  R, Endo  H  et al.  KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Valencia A (ed.), Bioinformatics. 2020;36:2251–2. 10.1093/bioinformatics/btz859. PubMed DOI PMC

Arora  DK. Chemotaxis of actinoplanes missouriensis zoospores to fungal conidia, chlamydospores and sclerotia. Microbiology. 1986;132:1657–63. 10.1099/00221287-132-6-1657. DOI

Baldrian  P, Zrůstová  P, Tláskal  V  et al.  Fungi associated with decomposing deadwood in a natural beech-dominated forest. Fungal Ecol. 2016;23:109–22. 10.1016/j.funeco.2016.07.001. DOI

Bellenger  JP, Darnajoux  R, Zhang  X  et al.  Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry. 2020;149:53–73. 10.1007/s10533-020-00666-7. DOI

Bolger  AM, Lohse  M, Usadel  B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. 10.1093/bioinformatics/btu170. PubMed DOI PMC

Bowman  SM, Free  SJ. The structure and synthesis of the fungal cell wall. Bioessays. 2006;28:799–808. 10.1002/bies.20441. PubMed DOI

Brabcová  V, Nováková  M, Davidová  A  et al.  Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytol. 2016;210:1369–81. 10.1111/nph.13849. PubMed DOI

Brabcová  V, Štursová  M, Baldrian  P. Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. Soil Biol Biochem. 2018;118:187–98. 10.1016/j.soilbio.2017.12.012. DOI

Brabcová  V, Tláskal  V, Lepinay  C  et al.  Fungal community development in decomposing fine deadwood is largely affected by microclimate. Front Microbiol. 2022;13:835274. 10.3389/fmicb.2022.835274. PubMed DOI PMC

Campitelli  E. Ggnewscale: Multiple Fill and Colour Scales in “Ggplot2.”. 2022. https://CRAN.R-project.org/package=ggnewscale (1 September 2023, date last accessed).

Caporaso  JG, Lauber  CL, Walters  WA  et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4. 10.1038/ismej.2012.8. PubMed DOI PMC

Charrad  M, Ghazzali  N, Boiteau  V  et al.  NbClust: an R package for determining the relevant number of clusters in a data set. J Stat Soft. 2014;61:1–36. 10.18637/jss.v061.i06. DOI

Chase  AB, Arevalo  P, Polz  MF  et al.  Evidence for ecological flexibility in the cosmopolitan genus curtobacterium. Front Microbiol. 2016;7. 10.3389/fmicb.2016.01874. PubMed DOI PMC

Covey  KR, De Mesquita  CPB, Oberle  B  et al.  Greenhouse trace gases in deadwood. Biogeochemistry. 2016;130:215–26. 10.1007/s10533-016-0253-1. DOI

Eddy  SR. Accelerated profile HMM searches. Pearson  WR (ed.), PLoS Comput Biol. 2011;7:e1002195. 10.1371/journal.pcbi.1002195. PubMed DOI PMC

El-Tarabily  KA. An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupin caused by Plectosporium tabacinum. Aust J Bot. 2003;51:257. 10.1071/BT02107. DOI

Eskalen  A, Stouthamer  R, Lynch  SC  et al.  Host range of fusarium dieback and its ambrosia beetle (Coleoptera: scolytinae) vector in Southern California. Plant Dis. 2013;97:938–51. 10.1094/PDIS-11-12-1026-RE. PubMed DOI

Feng  J-W, Liu  W-T, Chen  J-J  et al.  Biogeography and ecology of magnaporthales: a case study. Front Microbiol. 2021;12:654380. 10.3389/fmicb.2021.654380. PubMed DOI PMC

Fernandez  CW, Koide  RT. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol Biochem. 2014;77:150–7. 10.1016/j.soilbio.2014.06.026. DOI

Feron  R, Waterhouse  RM. Assessing species coverage and assembly quality of rapidly accumulating sequenced genomes. GigaScience. 2022;11:giac006. 10.1093/gigascience/giac006. PubMed DOI PMC

Filipiak  M, Weiner  J. How to make a beetle out of wood: multi-elemental stoichiometry of wood decay, xylophagy and fungivory. Wilson  RA (ed.), PLoS One. 2014;9:e115104. 10.1371/journal.pone.0115104. PubMed DOI PMC

Friess  N, Müller  JC, Aramendi  P  et al.  Arthropod communities in fungal fruitbodies are weaklystructured by climate and biogeography across European beech forests. Traveset  A (ed.), Divers Distrib. 2019;25:783–96. 10.1111/ddi.12882. DOI

Fukasawa  Y. Ecological impacts of fungal wood decay types: a review of current knowledge and future research directions. Ecol Res. 2021;36:910–31. 10.1111/1440-1703.12260. DOI

Gohar  D, Pent  M, Põldmaa  K  et al.  Bacterial community dynamics across developmental stages of fungal fruiting bodies. FEMS Microbiol Ecol. 2020;96:fiaa175. 10.1093/femsec/fiaa175. PubMed DOI

Gómez-Brandón  M, Probst  M, Siles  JA  et al.  Fungal communities and their association with nitrogen-fixing bacteria affect early decomposition of Norway spruce deadwood. Sci Rep. 2020;10:8025. 10.1038/s41598-020-64808-5. PubMed DOI PMC

Grabherr  MG, Haas  BJ, Yassour  M  et al.  Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol. 2011;29:644–52. 10.1038/nbt.1883. PubMed DOI PMC

Grigoriev  IV, Nikitin  R, Haridas  S  et al.  MycoCosm portal: gearing up for 1000 fungal genomes. Nucl Acids Res. 2014;42:D699–704. 10.1093/nar/gkt1183. PubMed DOI PMC

Harrington  TC. Ecology and evolution of mycophagous bark beetles and their fungal partners. In: Vega  FE, Blackwell  M (eds.), Ecological and Evolutionary Advances in Insect-Fungal Associations. New York: Oxford University Press, 2005, 257–91.

Heilmann-Clausen  J, Boddy  L. Inhibition and stimulation effects in communities of wood decay fungi: exudates from colonized wood influence growth by other species. Microb Ecol. 2005;49:399–406. 10.1007/s00248-004-0240-2. PubMed DOI

Hoppe  B, Kahl  T, Karasch  P  et al.  Network analysis reveals ecological links between N-Fixing Bacteria and Wood-Decaying Fungi. Desvaux  M (ed.), PLoS One. 2014;9:e88141. 10.1371/journal.pone.0088141. PubMed DOI PMC

Howard  FL, Currie  ME. Parasitism of myxomycete plasmodia on fungous mycelia. J Arnold Arbor. 1932a;13:438–47. 10.5962/p.185269. DOI

Howard  FL, Currie  ME. Parasitism of myxomycete plasmodia on the sporophores of hymenomycetes. J Arnold Arbor. 1932b;13:270–84. 10.5962/p.185255. DOI

Huang  L, Zhang  H, Wu  P  et al.  dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res. 2018;46:D516–21. 10.1093/nar/gkx894. PubMed DOI PMC

Huhndorf  SM, Greif  M, Mugambi  GK  et al.  Two new genera in the Magnaporthaceae, a new addition to Ceratosphaeria and two new species of Lentomitella. Mycologia. 2008;100:940–55. 10.3852/08-037. PubMed DOI

Kacprzyk  M, Bednarz  B, Kuźnik  E. Dead trees in beech stands of the Bieszczady National Park: quantitative and qualitative structure of associated macrofungi. Appl Ecol Env Res. 2014;12:325–44. 10.15666/aeer/1202_325344. DOI

Kaczmarczyk-Ziemba  A, Wagner  GK, Grzywnowicz  K  et al.  The microbiome profiling of fungivorous black tinder fungus beetle bolitophagus reticulatus reveals the insight into bacterial communities associated with larvae and adults. PeerJ. 2019;7:e6852. 10.7717/peerj.6852. PubMed DOI PMC

Kalitukha  L, Sari  M. Fascinating vital mushrooms. Tinder fungus (Fomes fomentarius (L.) Fr.) as a dietary supplement. Int J Res Stud Sci Eng Tech. 2019;6:1–9.

Kaltenpoth  M, Flórez  LV. Versatile and dynamic symbioses between insects and Burkholderia bacteria. Annu Rev Entomol. 2020;65:145–70. 10.1146/annurev-ento-011019-025025. PubMed DOI

Kanehisa  M.. KEGG: kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000;28:27–30. 10.1093/nar/28.1.27. PubMed DOI PMC

Kepler  RM, Maul  JE, Rehner  SA. Managing the plant microbiome for biocontrol fungi: examples from Hypocreales. Curr Opin Microbiol. 2017;37:48–53. 10.1016/j.mib.2017.03.006. PubMed DOI

Koide  RT, Malcolm  GM. N concentration controls decomposition rates of different strains of ectomycorrhizal fungi. Fungal Ecol. 2009;2:197–202. 10.1016/j.funeco.2009.06.001. DOI

Kolde  R. Pheatmap: pretty Heatmaps., 2019. https://CRAN.R-project.org/package=pheatmap (1 September 2023, date last accessed).

Kolundžić  M, Grozdanić  NĐ, Dodevska  M  et al.  Antibacterial and cytotoxic activities of wild mushroom fomes fomentarius (L.) Fr., polyporaceae. Ind Crops Prod. 2016;79:110–5. 10.1016/j.indcrop.2015.10.030. DOI

Koukol  O, Mourek  J, Janovský  Z  et al.  Do oribatid mites (Acari: oribatida) show a higher preference for ubiquitous vs. specialized saprotrophic fungi from pine litter?. Soil Biol Biochem. 2009;41:1124–31. 10.1016/j.soilbio.2009.02.018. DOI

Li  D, Liu  C-M, Luo  R  et al.  MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6. 10.1093/bioinformatics/btv033. PubMed DOI

Liao  Y, Smyth  GK, Shi  W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 2019;47:e47. 10.1093/nar/gkz114. PubMed DOI PMC

Liu  Y, Sun  Q, Li  J  et al.  Bacterial diversity among the fruit bodies of ectomycorrhizal and saprophytic fungi and their corresponding hyphosphere soils. Sci Rep. 2018;8:11672. 10.1038/s41598-018-30120-6. PubMed DOI PMC

López-Mondéjar  R, Brabcová  V, Štursová  M  et al.  Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling. ISME J. 2018;12:1768–78. 10.1038/s41396-018-0084-2. PubMed DOI PMC

López-Mondéjar  R, Tláskal  V, Větrovský  T  et al.  Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil. Soil Biol Biochem. 2020;148:107875. 10.1016/j.soilbio.2020.107875. DOI

Maechler  M, Rousseeuw  P, Struyf  A  et al.  Cluster: Cluster Analysis Basics and Extensions. 2022. https://CRAN.R-project.org/package=cluster (1 September 2023, date last accessed).

McFarlane  DJ, Aitken  EAB, Ridley  AW  et al.  The dietary relationships of Tribolium castaneum (Herbst) with microfungi. J Applied Entomology. 2021;145:158–69. 10.1111/jen.12830. DOI

Mihál  I, Cicák  A, Bucinova  K  Distribution, ecology and taxonomical notes to species of genera Hypomyces and Nectria (Hypocreales) in Slovakia. Mikologiia I Fitopatologiia. 2007;41:242.

Mukhin  VA, Voronin  PY. A new source of methane in boreal forests. Appl Biochem Microbiol. 2008;44:297–9. 10.1134/S0003683808030125. PubMed DOI

Mukhin  VA, Voronin  PY. Methanogenic activity of woody debris. Russ J Ecol. 2009;40:149–53. 10.1134/S1067413609030011. DOI

Müller  J, Engel  H, Blaschke  M. Assemblages of wood-inhabiting fungi related to silvicultural management intensity in beech forests in southern Germany. Eur J Forest Res. 2007;126:513–27. 10.1007/s10342-007-0173-7. DOI

Naegele  A, Reboux  G, Scherer  E  et al.  Fungal food choices of dermatophagoides farinae affect indoor fungi selection and dispersal. Int J Environ Health Res. 2013;23:91–5. 10.1080/09603123.2012.699029. PubMed DOI

Neuwirth  E. RColorBrewer: ColorBrewer Palettes. 2022. https://CRAN.R-project.org/package=RColorBrewer (1 September 2023, date last accessed).

Nones  S, Simões  F, Trindade  CS  et al.  Microbiome associated with the mycangia of female and male adults of the Ambrosia Beetle Platypus cylindrus Fab. (Coleoptera: curculionidae). Insects. 2021;12:881. 10.3390/insects12100881. PubMed DOI PMC

Økland  B. Canopy cover favours sporocarp-visiting beetles in spruce forest. Norw J Entomol. 2002;29–39.

Pent  M, Bahram  M, Põldmaa  K. Fruitbody chemistry underlies the structure of endofungal bacterial communities across fungal guilds and phylogenetic groups. ISME J. 2020;14:2131–41. 10.1038/s41396-020-0674-7. PubMed DOI PMC

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. 10.3389/fmicb.2017.00836. PubMed DOI PMC

Pylkkänen  R, Werner  D, Bishoyi  A  et al.  The complex structure of Fomes fomentarius represents an architectural design for high-performance ultralightweight materials. Sci Adv. 2023;9:eade5417. 10.1126/sciadv.ade5417. PubMed DOI PMC

Quast  C, Pruesse  E, Yilmaz  P  et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6. 10.1126/10.1093/nar/gks1219. PubMed DOI PMC

R Core Team . R: a Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2023. https://www.R-project.org/  (29 February 2024, date last accessed).

Ren  W, Penttilä  R, Kasanen  R  et al.  Bacteria community inhabiting heterobasidion fruiting body and associated wood of different decay classes. Front Microbiol. 2022;13:864619. 10.3389/fmicb.2022.864619. PubMed DOI PMC

Rho  M, Tang  H, Ye  Y. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 2010;38:e191. 10.1093/nar/gkq747. PubMed DOI PMC

Sari  M, Prange  A, Lelley  JI  et al.  Screening of beta-glucan contents in commercially cultivated and wild growing mushrooms. Food Chem. 2017;216:45–51. 10.1016/j.foodchem.2016.08.010. PubMed DOI

Schneider  K, Maraun  M. Feeding preferences among dark pigmented fungal taxa (“Dematiacea”) indicate limited trophic niche differentiation of oribatid mites (Oribatida, Acari). Pedobiologia. 2005;49:61–7. 10.1016/j.pedobi.2004.07.010. DOI

Schneider  K, Renker  C, Maraun  M. Oribatid mite (Acari, Oribatida) feeding on ectomycorrhizal fungi. Mycorrhiza. 2005;16:67–72. 10.1007/s00572-005-0015-8. PubMed DOI

Schwarze  F. Wood rotting fungi: fomes fomentarius (L.: fr.) Fr. Mycologist. 1994;8:32–4. 10.1016/S0269-915X(09)80679-4. DOI

Seibold  S, Müller  J, Baldrian  P  et al.  Fungi associated with beetles dispersing from dead wood—Let's take the beetle bus! Fungal Ecol. 2019;39:100–8. 10.1016/j.funeco.2018.11.016. DOI

Shipunov  A, Murrell  P, D'Orazio  M  et al.  Shipunov: Miscellaneous Functions from Alexey Shipunov. 2023. https://CRAN.R-project.org/package=shipunov (1 September 2023, date last accessed).

Simonsohn  U, Gruson  H. Groundhog: Version-Control for CRAN, GitHub, and GitLab Packages. 2023. https://CRAN.R-project.org/package=groundhog (1 September 2023, date last accessed).

Sinha  RN. Development and mortality of tribolium castaneum and T. confusum (Coleoptera: tenebrionidae) on seed-borne Fungi1. Ann Entomol Soc Am. 1966;59:192–201. 10.1093/aesa/59.1.192. DOI

Skelton  J, Jusino  MA, Carlson  PS  et al.  Relationships among wood-boring beetles, fungi, and the decomposition of forest biomass. Mol Ecol. 2019;28:4971–86. 10.1111/mec.15263. PubMed DOI

Slowikowski  K. ggrepel: automatically position non-overlapping text labels with “ggplot2”. 2021. https://CRAN.R-project.org/package=ggrepel (1 September 2023, date last accessed).

Song  J, Song  J, Liang  J-F  et al.  Fungal systematics and evolution: FUSE 5. Sydowia An International Journal of Mycology. 2019;71:141–245. 10.12905/0380.sydowia71-2019-0141. PubMed DOI PMC

Stoyanova  M, Pavlina  I, Moncheva  P  et al.  Biodiversity and incidence of Burkholderia species. Biotechnol Biotechnol Equip. 2007;21:306–10. 10.1080/13102818.2007.10817465. DOI

Štursová  M, Šnajdr  J, Cajthaml  T  et al.  When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. ISME J. 2014;8:1920–31. 10.1038/ismej.2014.37. PubMed DOI PMC

Thunes  K. The coleopteran fauna of Piptoporus betulinus and Fomes fomentarius (Aphyllophorales: Polyporaceae) in western Norway. Entomol Fennica. 1994;5:157–68. 10.33338/ef.83813. DOI

Thunes  KH, Willassen  E. Species composition of beetles (Coleoptera) in the bracket fungi Piptoporus betulinus and Fomes fomentarius (Aphyllophorales: Polyporaceae): an explorative approach with canonical correspondence analysis. Msystems. 2021;6:471–86. 10.1080/00222939700770241. DOI

Tláskal  V, Brabcová  V, Větrovský  T  et al.  Complementary roles of wood-inhabiting fungi and bacteria facilitate deadwood decomposition. Faust  K (ed.), Msystems. 2021;6:e01078–20. 10.1128/mSystems.01078-20. PubMed DOI PMC

Valette  N, Legout  A, Goodell  B  et al.  Impact of Norway spruce pre-degradation stages induced by Gloeophyllum trabeum on fungal and bacterial communities. Fungal Ecol. 2023;61:101188. 10.1016/j.funeco.2022.101188. DOI

Vries  Ad, Ripley  BD.  Ggdendro: Create Dendrograms and Tree Diagrams Using “Ggplot2.”. 2022. https://CRAN.R-project.org/package=ggdendro (1 September 2023, date last accessed).

Wickham  H. Ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York, 2016. https://ggplot2.tidyverse.org (1 September 2023, date last accessed).

Wickham  H. Stringr: Simple, Consistent Wrappers for Common String Operations. 2022. https://CRAN.R-project.org/package=stringr (1 September 2023, date last accessed).

Wilke  CO. Cowplot: Streamlined Plot Theme and Plot Annotations for “Ggplot2.”. 2020. https://CRAN.R-project.org/package=cowplot (1 September 2023, date last accessed).

Yu  G.  Ggplotify: Convert Plot to “grob” or “Ggplot” Object. 2021. https://CRAN.R-project.org/package=ggplotify (1 September 2023, date last accessed).

Zhang  N, Castlebury  LA, Miller  AN  et al.  An overview of the systematics of the sordariomycetes based on a four-gene phylogeny. Mycologia. 2006;98:1076–87. 10.1080/15572536.2006.11832635. PubMed DOI