Advertisement

Home-Field Advantage in Wood Decomposition Is Mainly Mediated by Fungal Community Shifts at “Home” Versus “Away”

  • Witoon PurahongEmail author
  • Tiemo Kahl
  • Dirk Krüger
  • François Buscot
  • Björn HoppeEmail author
Soil Microbiology

Abstract

The home-field advantage (HFA) hypothesis has been used intensively to study leaf litter decomposition in various ecosystems. However, the HFA in woody substrates is still unexplored. Here, we reanalyzed and integrated existing datasets on various groups of microorganisms collected from natural deadwood of two temperate trees, Fagus sylvatica and Picea abies, from forests in which one or other of these species dominates but where both are present. Our aims were (i) to test the HFA hypothesis on wood decomposition rates of these two temperate tree species, and (ii) to investigate if HFA hypothesis can be explained by diversity and community composition of bacteria and in detail N-fixing bacteria (as determined by molecular 16S rRNA and nifH gene amplification) and fungi (as determined by molecular ITS rRNA amplification and sporocarp surveys). Our results showed that wood decomposition rates were accelerated at “home” versus “away” by 38.19% ± 20.04% (mean ± SE). We detected strong changes in fungal richness (increase 36–50%) and community composition (RANOSIM = 0.52–0.60, P < 0.05) according to HFA hypothesis. The changes of fungi were much stronger than for total bacteria and nitrogen fixing for both at richness and community composition levels. In conclusion, our results support the HFA hypothesis in deadwood: decomposition rate is accelerated at home due to specialization of fungal communities produced by the plant community above them. Furthermore, the higher richness of fungal sporocarps and nitrogen-fixing bacteria (nifH) may stimulate or at least stabilize wood decomposition rates at “home” versus “away.”

Keywords

Home-field advantage (HFA) Microbial communities Nitrogen-fixing bacteria Deadwood Wood decay rate Decomposition Next-generation sequencing 

Notes

Acknowledgements

We thank the managers of the three Exploratories, Swen Renner, Sonja Gockel, and Andreas Hemp, and all former managers for their work in maintaining the plot and project infrastructure; Simone Pfeffer, Maren Gleisberg, and Christiane Fischer, and all members at BEO for giving support through the central office; Jens Nieschulze for managing the central data base; and Markus Fischer, Eduard Linsenmair, Dominik Hessenmöller, Daniel Prati, Ingo Schöning, François Buscot, Ernst-Detlef Schulze, Wolfgang W. Weisser, and the late Elisabeth Kalko for their role in setting up the Biodiversity Exploratories project.

Availability of Data and Material

The dataset analyzed during this study are included in this manuscript as Supplementary material files. The raw sequence data for the ITS and 16S pyrosequencing datasets are available from the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/Traces/study/) under experiments SRX589508 and SRX589509, respectively. New nifH nucleotide sequences and their MOTU (molecular operational taxonomic unit) assignments are available under accession numbers HF559482-HF560561.

Authors’ Contributions

WP conceived the ideas. TK, DK, and BH collected the data. WP, BH, and FB designed methodology. WP and BH analyzed data; WP and BH led the writing of the manuscript with substantial contributions of all co-authors.

Funding

The work has been (partly) funded by the DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories” (KR 3587/1-1, KR 3587/3-2, BU 941/17-1).

Compliance with Ethical Standards

Ethics Statement

Field work permits were issued by the responsible state environmental offices of Baden-Württemberg, Thüringen, and Brandenburg (according to § 72 BbgNatSchG).

Consent for Publication

The manuscript does not contain any individual person’s data in any form. The image contained in this manuscript was generated by the authors.

Competing Interests

The authors declare that they have no competing interests.

Supplementary material

248_2019_1334_MOESM1_ESM.pdf (382 kb)
ESM 1 (PDF 381 kb)
248_2019_1334_MOESM2_ESM.xlsx (50 kb)
ESM 2 (XLSX 50 kb)

References

  1. 1.
    Purahong W, Arnstadt T, Kahl T et al (2016) Are correlations between deadwood fungal community structure, wood physico-chemical properties and lignin-modifying enzymes stable across different geographical regions? Fungal Ecol. 22:98–105.  https://doi.org/10.1016/j.funeco.2016.01.002 CrossRefGoogle Scholar
  2. 2.
    Rajala T, Peltoniemi M, Pennanen T, Mäkipää R (2012) Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies [L.] Karst.) logs in boreal forests. FEMS Microbiol. Ecol. 81:494–505.  https://doi.org/10.1111/j.1574-6941.2012.01376.x CrossRefGoogle Scholar
  3. 3.
    Arnstadt T, Hoppe B, Kahl T et al (2016) Patterns of laccase and peroxidases in coarse woody debris of Fagus sylvatica, Picea abies and Pinus sylvestris and their relation to different wood parameters. Eur. J. For. Res. 135:109–124.  https://doi.org/10.1007/s10342-015-0920-0 CrossRefGoogle Scholar
  4. 4.
    Hoppe B, Kahl T, Karasch P et al (2014) Network analysis reveals ecological links between N-fixing bacteria and wood-decaying fungi. PLoS One 9:e88141.  https://doi.org/10.1371/journal.pone.0088141 CrossRefPubMedCentralGoogle Scholar
  5. 5.
    Hoppe B, Krger K, Kahl T et al (2015) A pyrosequencing insight into sprawling bacterial diversity and community dynamics in decaying deadwood logs of Fagus sylvatica and Picea abies. Sci. Rep. 5(9456).  https://doi.org/10.1038/srep09456
  6. 6.
    Mäkipää R, Leppänen SM, Sanz Munoz S et al (2018) Methanotrophs are core members of the diazotroph community in decaying Norway spruce logs. Soil Biol. Biochem. 120:230–232.  https://doi.org/10.1016/j.soilbio.2018.02.012 CrossRefGoogle Scholar
  7. 7.
    Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database J Biol Databases Curation 2014.  https://doi.org/10.1093/database/bau001
  8. 8.
    Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ. Microbiol. 13:1790–1799.  https://doi.org/10.1111/j.1462-2920.2011.02488.x CrossRefGoogle Scholar
  9. 9.
    Cornelissen JHC, Sass-Klaassen U, Poorter L et al (2012) Controls on coarse wood decay in temperate tree species: birth of the LOGLIFE experiment. Ambio 41:231–245.  https://doi.org/10.1007/s13280-012-0304-3 CrossRefPubMedCentralGoogle Scholar
  10. 10.
    Hoppe B, Purahong W, Wubet T et al (2016) Linking molecular deadwood-inhabiting fungal diversity and community dynamics to ecosystem functions and processes in Central European forests. Fungal Divers. 77:367–379.  https://doi.org/10.1007/s13225-015-0341-x CrossRefGoogle Scholar
  11. 11.
    Binkley D, Giardina C (1998) Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42:89–106CrossRefGoogle Scholar
  12. 12.
    Ushio M, Kitayama K, Balser TC (2010) Tree species effects on soil enzyme activities through effects on soil physicochemical and microbial properties in a tropical montane forest on Mt. Kinabalu, Borneo. Pedobiologia 53:227–233.  https://doi.org/10.1016/j.pedobi.2009.12.003 CrossRefGoogle Scholar
  13. 13.
    Lamit LJ, Busby PE, Lau MK et al (2015) Tree genotype mediates covariance among communities from microbes to lichens and arthropods. J. Ecol. 103:840–850.  https://doi.org/10.1111/1365-2745.12416 CrossRefGoogle Scholar
  14. 14.
    Purahong W, Durka W, Fischer M et al (2016) Tree species, tree genotypes and tree genotypic diversity levels affect microbe-mediated soil ecosystem functions in a subtropical forest. Sci. Rep. 6(36672).  https://doi.org/10.1038/srep36672
  15. 15.
    Veen GF (Ciska), Freschet GT, Ordonez A, Wardle DA (2015) Litter quality and environmental controls of home-field advantage effects on litter decomposition. Oikos 124:187–195.  https://doi.org/10.1111/oik.01374
  16. 16.
    Ayres E, Steltzer H, Simmons BL et al (2009) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol. Biochem. 41:606–610.  https://doi.org/10.1016/j.soilbio.2008.12.022 CrossRefGoogle Scholar
  17. 17.
    Li Y-B, Li Q, Yang J-J et al (2017) Home-field advantages of litter decomposition increase with increasing N deposition rates: a litter and soil perspective. Funct. Ecol. 31:1792–1801.  https://doi.org/10.1111/1365-2435.12863 CrossRefGoogle Scholar
  18. 18.
    Veen GF, Sundqvist MK, Wardle DA (2015) Environmental factors and traits that drive plant litter decomposition do not determine home-field advantage effects. Funct Ecol 29:981–991.  https://doi.org/10.1111/1365-2435.12421 CrossRefGoogle Scholar
  19. 19.
    Purahong W, Wubet T, Lentendu G et al (2016) Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition. Mol. Ecol.  https://doi.org/10.1111/mec.13739
  20. 20.
    Purahong W, Stempfhuber B, Lentendu G et al (2015) Influence of commonly used primer systems on automated ribosomal intergenic spacer analysis of bacterial communities in environmental samples. PLoS One 10:e0118967.  https://doi.org/10.1371/journal.pone.0118967 CrossRefPubMedCentralGoogle Scholar
  21. 21.
    Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu. Rev. Ecol. Syst. 33:1–23.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150507 CrossRefGoogle Scholar
  22. 22.
    Müller J, Bütler R (2010) A review of habitat thresholds for dead wood: a baseline for management recommendations in European forests. Eur. J. For. Res. 129:981–992.  https://doi.org/10.1007/s10342-010-0400-5 CrossRefGoogle Scholar
  23. 23.
    Purahong W, Hoppe B, Kahl T et al (2014) Changes within a single land-use category alter microbial diversity and community structure: molecular evidence from wood-inhabiting fungi in forest ecosystems. J. Environ. Manag. 139:109–119.  https://doi.org/10.1016/j.jenvman.2014.02.031 CrossRefGoogle Scholar
  24. 24.
    Bässler C, Ernst R, Cadotte M, Heibl C, Müller J (2014) Near-to-nature logging influences fungal community assembly processes in a temperate forest. J. Appl. Ecol. 51:939–948.  https://doi.org/10.1111/1365-2664.12267 CrossRefGoogle Scholar
  25. 25.
    Fischer M, Bossdorf O, Gockel S et al (2010) Implementing large-scale and long-term functional biodiversity research: the Biodiversity Exploratories. Basic Appl Ecol 11:473–485.  https://doi.org/10.1016/j.baae.2010.07.009 CrossRefGoogle Scholar
  26. 26.
    Luyssaert S, Hessenmöller D, von Lüpke N et al (2011) Quantifying land use and disturbance intensity in forestry, based on the self-thinning relationship. Ecol. Appl. 21:3272–3284.  https://doi.org/10.1890/10-2395.1 CrossRefGoogle Scholar
  27. 27.
    Hessenmöller D, Nieschulze J, Von Lüpke N, Schulze E-D (2011) Identification of forest management types from ground-based and remotely sensed variables and the effects of forest management on forest structure and composition. Forstarchiv 82:171–183.  https://doi.org/10.4432/0300-4112-82-171
  28. 28.
    Müller-Using S, Bartsch N (2009) Decay dynamic of coarse and fine woody debris of a beech (Fagus sylvatica L.) forest in Central Germany. Eur. J. For. Res. 128:287–296.  https://doi.org/10.1007/s10342-009-0264-8 CrossRefGoogle Scholar
  29. 29.
    Urbanová M, Šnajdr J, Baldrian P (2015) Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol. Biochem. 84:53–64.  https://doi.org/10.1016/j.soilbio.2015.02.011 CrossRefGoogle Scholar
  30. 30.
    Jacob M, Viedenz K, Polle A, Thomas FM (2010) Leaf litter decomposition in temperate deciduous forest stands with a decreasing fraction of beech (Fagus sylvatica). Oecologia 164:1083–1094.  https://doi.org/10.1007/s00442-010-1699-9 CrossRefPubMedCentralGoogle Scholar
  31. 31.
    Konôpka B, Pajtík J, Noguchi K, Lukac M (2013) Replacing Norway spruce with European beech: a comparison of biomass and net primary production patterns in young stands. For. Ecol. Manag. 302:185–192.  https://doi.org/10.1016/j.foreco.2013.03.026 CrossRefGoogle Scholar
  32. 32.
    Ammer C, Bickel E, Kölling C (2008) Converting Norway spruce stands with beech - a review of arguments and techniques. Austrian J For Sci 125:3–26Google Scholar
  33. 33.
    Purahong W, Kahl T, Schloter M et al (2014) Comparing fungal richness and community composition in coarse woody debris in Central European beech forests under three types of management. Mycol. Prog. 13:959–964.  https://doi.org/10.1007/s11557-013-0954-y CrossRefGoogle Scholar
  34. 34.
    Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinforma Oxf Engl 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefGoogle Scholar
  35. 35.
    Kahl T, Mund M, Bauhus J, Schulze E-D (2012) Dissolved organic carbon from European beech logs: patterns of input to and retention by surface soil. Ecoscience 19:364–373.  https://doi.org/10.2980/19-4-3501 CrossRefGoogle Scholar
  36. 36.
    Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol. Ecol. 19:5555–5565.  https://doi.org/10.1111/j.1365-294X.2010.04898.x CrossRefGoogle Scholar
  37. 37.
    Purahong W, Wubet T, Krüger D, Buscot F (2018) Molecular evidence strongly supports deadwood-inhabiting fungi exhibiting unexpected tree species preferences in temperate forests. ISME J 12:289–295.  https://doi.org/10.1038/ismej.2017.177 CrossRefGoogle Scholar
  38. 38.
    Purahong W, Wubet T, Kahl T et al (2018) Increasing N deposition impacts neither diversity nor functions of deadwood-inhabiting fungal communities, but adaptation and functional redundancy ensure ecosystem function. Environ. Microbiol. 20:1693–1710.  https://doi.org/10.1111/1462-2920.14081 CrossRefGoogle Scholar
  39. 39.
    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:9Google Scholar
  40. 40.
    Goldmann K, Schöning I, Buscot F, Wubet T (2015) Forest management type influences diversity and community composition of soil fungi across temperate forest ecosystems. Front. Microbiol. 6.  https://doi.org/10.3389/fmicb.2015.01300
  41. 41.
    Greaves H (1971) The bacterial factor in wood decay. Wood Sci. Technol. 5:6–16.  https://doi.org/10.1007/BF00363116 CrossRefGoogle Scholar
  42. 42.
    Kielak AM, Scheublin TR, Mendes LW et al (2016) Bacterial community succession in pine-wood decomposition. Terr Microbiol 231.  https://doi.org/10.3389/fmicb.2016.00231
  43. 43.
    Austin AT, Vivanco L, González-Arzac A, Pérez LI (2014) There’s no place like home? An exploration of the mechanisms behind plant litter–decomposer affinity in terrestrial ecosystems. New Phytol. 204:307–314.  https://doi.org/10.1111/nph.12959 CrossRefGoogle Scholar
  44. 44.
    Freschet GT, Aerts R, Cornelissen JHC (2012) Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis. J. Ecol. 100:619–630.  https://doi.org/10.1111/j.1365-2745.2011.01943.x CrossRefGoogle Scholar
  45. 45.
    Purahong W, Kapturska D, Pecyna MJ et al (2014) Influence of different forest system management practices on leaf litter decomposition rates, nutrient dynamics and the activity of ligninolytic enzymes: a case study from Central European forests. PLoS One 9:e93700.  https://doi.org/10.1371/journal.pone.0093700 CrossRefPubMedCentralGoogle Scholar
  46. 46.
    Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J. Ecol. 96:727–736.  https://doi.org/10.1111/j.1365-2745.2008.01393.x CrossRefGoogle Scholar
  47. 47.
    Fukasawa Y, Osono T, Takeda H (2009) Effects of attack of saprobic fungi on twig litter decomposition by endophytic fungi. Ecol. Res. 24:1067–1073.  https://doi.org/10.1007/s11284-009-0582-9 CrossRefGoogle Scholar
  48. 48.
    Kuuskeri J, Mäkelä MR, Isotalo J et al (2015) Lignocellulose-converting enzyme activity profiles correlate with molecular systematics and phylogeny grouping in the incoherent genus Phlebia (Polyporales, Basidiomycota). BMC Microbiol. 15:217.  https://doi.org/10.1186/s12866-015-0538-x CrossRefPubMedCentralGoogle Scholar
  49. 49.
    Kinnunen A, Maijala P, Järvinen P, Hatakka A (2017) Improved efficiency in screening for lignin-modifying peroxidases and laccases of basidiomycetes. Curr Biotechnol 6:105–115CrossRefGoogle Scholar
  50. 50.
    Vrsanska M, Voberkova S, Langer V et al (2016) Induction of laccase, lignin peroxidase and manganese peroxidase activities in white-rot fungi using copper complexes. Molecules 21:1553.  https://doi.org/10.3390/molecules21111553 CrossRefPubMedCentralGoogle Scholar
  51. 51.
    Rayner ADM, Boddy L (1988) Fungal decomposition of wood: its biology and ecology. John Wiley & Sons Ltd., Chichester, Sussex, United KingdomGoogle Scholar
  52. 52.
    Song Z, Kennedy PG, Liew FJ, Schilling JS (2017) Fungal endophytes as priority colonizers initiating wood decomposition. Funct. Ecol. 31:407–418.  https://doi.org/10.1111/1365-2435.12735 CrossRefGoogle Scholar
  53. 53.
    Parfitt D, Hunt J, Dockrell D et al (2010) Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol. 3:338–346.  https://doi.org/10.1016/j.funeco.2010.02.001 CrossRefGoogle Scholar
  54. 54.
    Hallenberg N, Kúffer N (2001) Long-distance spore dispersal in wood-inhabiting Basidiomycetes. Nord. J. Bot. 21:431–436.  https://doi.org/10.1111/j.1756-1051.2001.tb00793.x CrossRefGoogle Scholar
  55. 55.
    Dobbs CG (1942) On the primary dispersal and isolation of fungal spores. New Phytol. 41:63–69.  https://doi.org/10.1111/j.1469-8137.1942.tb07060.x CrossRefGoogle Scholar
  56. 56.
    Andrade D, Pan Z, Dannevik W, Zidek J (2009) Modeling soybean rust spore escape from infected canopies: model description and preliminary results. J. Appl. Meteorol. Climatol. 48:789–803.  https://doi.org/10.1175/2008JAMC1917.1 CrossRefGoogle Scholar
  57. 57.
    Edman M, Gustafsson M, Stenlid J et al (2004) Spore deposition of wood-decaying fungi: importance of landscape composition. Ecography 27:103–111.  https://doi.org/10.1111/j.0906-7590.2004.03671.x CrossRefGoogle Scholar
  58. 58.
    Konôpka B, Pajtík J, Marušák R et al (2016) Specific leaf area and leaf area index in developing stands of Fagus sylvatica L. and Picea abies Karst. For. Ecol. Manag. 364:52–59.  https://doi.org/10.1016/j.foreco.2015.12.005 CrossRefGoogle Scholar
  59. 59.
    Floren A, Krüger D, Müller T et al (2015) Diversity and interactions of wood-inhabiting fungi and beetles after deadwood enrichment. PLoS One 10:e0143566.  https://doi.org/10.1371/journal.pone.0143566 CrossRefPubMedCentralGoogle Scholar
  60. 60.
    Valentín L, Rajala T, Peltoniemi M et al (2014) Loss of diversity in wood-inhabiting fungal communities affects decomposition activity in Norway spruce wood. Terr Microbiol 5(230).  https://doi.org/10.3389/fmicb.2014.00230
  61. 61.
    Yang Y, Schaefer DA, Liu W, et al (2016) Higher fungal diversity in dead wood is correlated with lower CO2 emissions in a natural forest. bioRxiv 51235.  https://doi.org/10.1101/051235
  62. 62.
    Weißhaupt P, Pritzkow W, Noll M (2011) Nitrogen metabolism of wood decomposing basidiomycetes and their interaction with diazotrophs as revealed by IRMS. Int. J. Mass Spectrom. 307:225–231.  https://doi.org/10.1016/j.ijms.2010.12.011 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.UFZ-Helmholtz Centre for Environmental Research, Department of Soil EcologyHalle (Saale)Germany
  2. 2.Faculty of Environment and Natural Resources, Chair of SilvicultureUniversity of FreiburgFreiburg i. Brsg.Germany
  3. 3.UNESCO Biosphere Reserve Thuringian ForestSchmiedefeld am RennsteigGermany
  4. 4.German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-LeipzigLeipzigGermany
  5. 5.Julius Kühn-Institute, Institute for National and International Plant HealthBraunschweigGermany

Personalised recommendations