Factors Controlling Dead Wood Decomposition in an Old-Growth Temperate Forest in Central Europe
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
project LTC20073
the Ministry of Education, Youth and Sports of the Czech Republic
PubMed
35887430
PubMed Central
PMC9325057
DOI
10.3390/jof8070673
PII: jof8070673
Knihovny.cz E-zdroje
- Klíčová slova
- chemical properties, extracellular enzymes, fungal biomass, fungal community, respiration, structural equation modeling,
- Publikační typ
- časopisecké články MeSH
Dead wood represents an important pool of carbon and nitrogen in forest ecosystems. This source of soil organic matter has diverse ecosystem functions that include, among others, carbon and nitrogen cycling. However, information is limited on how deadwood properties such as chemical composition, decomposer abundance, community composition, and age correlate and affect decomposition rate. Here, we targeted coarse dead wood of beech, spruce, and fir, namely snags and tree trunks (logs) in an old-growth temperate forest in central Europe; measured their decomposition rate as CO2 production in situ; and analyzed their relationships with other measured variables. Respiration rate of dead wood showed strong positive correlation with acid phosphatase activity and negative correlation with lignin content. Fungal biomass (ergosterol content) and moisture content were additional predictors. Our results indicate that dead wood traits, including tree species, age, and position (downed/standing), affected dead wood chemical properties, microbial biomass, moisture condition, and enzyme activity through changes in fungal communities and ultimately influenced the decomposition rate of dead wood.
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Seibold S., Rammer W., Hothorn T., Seidl R., Ulyshen M.D., Lorz J., Cadotte M.W., Lindenmayer D.B., Adhikari Y.P., Aragón R., et al. The Contribution of Insects to Global Forest Deadwood Decomposition. Nature. 2021;597:77–81. doi: 10.1038/s41586-021-03740-8. PubMed DOI
Stokland J.N., Siitonen J., Jonsson B.G. Biodiversity in Dead Wood. Cambridge University Press; Cambridge, UK: 2012.
Shi Z., Allison S.D., He Y., Levine P.A., Hoyt A.M., Beem-Miller J., Zhu Q., Wieder W.R., Trumbore S., Randerson J.T. The Age Distribution of Global Soil Carbon Inferred from Radiocarbon Measurements. Nat. Geosci. 2020;13:555–559. doi: 10.1038/s41561-020-0596-z. DOI
Hicks W.T. Ph.D. Thesis. Oregon State University; Corvallis, OR, USA: 2000. Modeling Nitrogen Fixation in Dead Wood; p. 9983428.
Lajtha K. Nutrient Retention and Loss during Ecosystem Succession: Revisiting a Classic Model. Ecology. 2020;101:e02896. doi: 10.1002/ecy.2896. PubMed DOI
Tláskal V., Brabcová V., Větrovský T., Jomura M., López-Mondéjar R., Monteiro M.O.L., Saraiva P.J., Human Z.R., Cajthaml T., Nunes da Rocha U., et al. Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition. mSystems. 2021;6:e01078-20. doi: 10.1128/mSystems.01078-20. PubMed DOI PMC
Kahl T., Arnstadt T., Baber K., Bässler C., Bauhus J., Borken W., Buscot F., Floren A., Heibl C., Hessenmöller D., et al. Wood Decay Rates of 13 Temperate Tree Species in Relation to Wood Properties, Enzyme Activities and Organismic Diversities. For. Ecol. Manag. 2017;391:86–95. doi: 10.1016/j.foreco.2017.02.012. DOI
Weedon J.T., Cornwell W.K., Cornelissen J.H.C., Zanne A.E., Wirth C., Coomes D.A. Global Meta-Analysis of Wood Decomposition Rates: A Role for Trait Variation among Tree Species? Ecol. Lett. 2009;12:45–56. doi: 10.1111/j.1461-0248.2008.01259.x. PubMed DOI
Yatskov M., Harmon M.E., Krankina O.N. A Chronosequence of Wood Decomposition in the Boreal Forests of Russia. Can. J. For. Res. 2003;33:1211–1226. doi: 10.1139/x03-033. DOI
Boulanger Y., Sirois L. Postfire Dynamics of Black Spruce Coarse Woody Debris in Northern Boreal Forest of Quebec. Can. J. For. Res. 2006;36:1770–1780. doi: 10.1139/x06-070. DOI
Bond-Lamberty B., Wang C., Gower S.T. Annual Carbon Flux from Woody Debris for a Boreal Black Spruce Fire Chronosequence. J. Geophys. Res. 2002;107:WFX 1-1–WFX 1-10. doi: 10.1029/2001JD000839. DOI
Bond-Lamberty B., Gower S.T. Decomposition and Fragmentation of Coarse Woody Debris: Re-Visiting a Boreal Black Spruce Chronosequence. Ecosystems. 2008;11:831–840. doi: 10.1007/s10021-008-9163-y. DOI
Herrmann S., Bauhus J. Effects of Moisture, Temperature and Decomposition Stage on Respirational Carbon Loss from Coarse Woody Debris (CWD) of Important European Tree Species. Scand. J. For. Res. 2012;28:346–357. doi: 10.1080/02827581.2012.747622. DOI
Berg B., McClaugherty C. Plant Litter, Decomposition, Humus Formation, Carbon Sequestration. Springer; Berlin/Heidelberg, Germany: 2013.
Bradford M.A., Warren R.J., Baldrian P., Crowther T.W., Maynard D.S., Oldfield E.E., Wieder W.R., Wood S.A., King J.R. Climate Fails to Predict Wood Decomposition at Regional Scales. Nat. Clim. Chang. 2014;4:625–630. doi: 10.1038/nclimate2251. DOI
Fukami T., Dickie I.A., Paula Wilkie J., Paulus B.C., Park D., Roberts A., Buchanan P.K., Allen R.B. Assembly History Dictates Ecosystem Functioning: Evidence from Wood Decomposer Communities. Ecol. Lett. 2010;13:675–684. doi: 10.1111/j.1461-0248.2010.01465.x. PubMed DOI
Chave J., Muller-Landau H.C., Baker T.R., Easdale T.A., Steege H., Webb C.O. Regional and Phylogenetic Variation of Wood Density across 2456 Neotropical Tree Species. Ecol. Appl. 2006;16:2356–2367. doi: 10.1890/1051-0761(2006)016[2356:RAPVOW]2.0.CO;2. PubMed DOI
Noll L., Leonhardt S., Arnstadt T., Hoppe B., Poll C., Matzner E., Hofrichter M., Kellner H. Fungal Biomass and Extracellular Enzyme Activities in Coarse Woody Debris of 13 Tree Species in the Early Phase of Decomposition. For. Ecol. Manag. 2016;378:181–192. doi: 10.1016/j.foreco.2016.07.035. DOI
Leonhardt S., Hoppe B., Stengel E., Noll L., Moll J., Bässler C., Dahl A., Buscot F., Hofrichter M., Kellner H. Molecular Fungal Community and Its Decomposition Activity in Sapwood and Heartwood of 13 Temperate European Tree Species. PLoS ONE. 2019;14:e0212120. doi: 10.1371/journal.pone.0212120. PubMed DOI PMC
Song Z., Kennedy P.G., Liew F.J., Schilling J.S. Fungal Endophytes as Priority Colonizers Initiating Wood Decomposition. Funct. Ecol. 2017;31:407–418. doi: 10.1111/1365-2435.12735. DOI
Wang L., Ren L., Li C., Gao C., Liu X., Wang M., Luo Y. Effects of Endophytic Fungi Diversity in Different Coniferous Species on the Colonization of Sirex Noctilio (Hymenoptera: Siricidae) Sci. Rep. 2019;9:5077. doi: 10.1038/s41598-019-41419-3. PubMed DOI PMC
Bradford M.A., Maynard D.S., Crowther T.W., Frankson P.T., Mohan J.E., Steinrueck C., Veen G.F., King J.R., Warren R.J., II Belowground Community Turnover Accelerates the Decomposition of Standing Dead Wood. Ecology. 2021;102:e03484. doi: 10.1002/ecy.3484. PubMed DOI
Meier C.L., Rapp J., Bowers R.M., Silman M., Fierer N. Fungal Growth on a Common Wood Substrate across a Tropical Elevation Gradient: Temperature Sensitivity, Community Composition, and Potential for above-Ground Decomposition. Soil Biol. Biochem. 2010;42:1083–1090. doi: 10.1016/j.soilbio.2010.03.005. DOI
Rajala T., Peltoniemi M., Hantula J., Mäkipää R., Pennanen T. RNA Reveals a Succession of Active Fungi during the Decay of Norway Spruce Logs. Fungal Ecol. 2011;4:437–448. doi: 10.1016/j.funeco.2011.05.005. DOI
Folman L.B., Klein Gunnewiek P.J.A., Boddy L., De Boer W. Impact of White-Rot Fungi on Numbers and Community Composition of Bacteria Colonizing Beech Wood from Forest Soil. FEMS Microbiol. Ecol. 2008;63:181–191. doi: 10.1111/j.1574-6941.2007.00425.x. PubMed DOI
Hiscox J., Savoury M., Vaughan I.P., Müller C.T., Boddy L. Antagonistic Fungal Interactions Influence Carbon Dioxide Evolution from Decomposing Wood. Fungal Ecol. 2015;14:24–32. doi: 10.1016/j.funeco.2014.11.001. DOI
Odriozola I., Abrego N., Tláskal V., Zrůstová P., Morais D., Větrovský T., Ovaskainen O., Baldrian P. Fungal Communities Are Important Determinants of Bacterial Community Composition in Deadwood. mSystems. 2021;6:e01017-20. doi: 10.1128/mSystems.01017-20. PubMed DOI PMC
Gómez-Brandón M., Probst M., Siles J.A., Peintner U., Bardelli T., Egli M., Insam H., Ascher-Jenull J. Fungal Communities and Their Association with Nitrogen-Fixing Bacteria Affect Early Decomposition of Norway Spruce Deadwood. Sci. Rep. 2020;10:8025. doi: 10.1038/s41598-020-64808-5. PubMed DOI PMC
Sinsabaugh R.L., Antibus R.K., Linkins A.E. An Enzymic Approach to the Analysis of Microbial Activity during Plant Litter Decomposition. Agric. Ecosyst. Environ. 1991;34:43–54. doi: 10.1016/0167-8809(91)90092-C. DOI
Sinsabaugh R.L., Antibus R.K., Linkins A.E., McClaugherty C.A., Rayburn L., Repert D., Weiland T. Wood Decomposition over a First-Order Watershed: Mass Loss as a Function of Lignocellulase Activity. Soil Biol. Biochem. 1992;24:743–749. doi: 10.1016/0038-0717(92)90248-V. DOI
Sinsabaugh R.S. Enzymic Analysis of Microbial Pattern and Process. Biol. Fertil. Soils. 1994;17:69–74. doi: 10.1007/BF00418675. DOI
A’Bear A.D., Jones T.H., Kandeler E., Boddy L. Interactive Effects of Temperature and Soil Moisture on Fungal-Mediated Wood Decomposition and Extracellular Enzyme Activity. Soil Biol. Biochem. 2014;70:151–158. doi: 10.1016/j.soilbio.2013.12.017. DOI
Wang G., Post W.M., Mayes M.A., Frerichs J.T., Sindhu J. Parameter Estimation for Models of Ligninolytic and Cellulolytic Enzyme Kinetics. Soil Biol. Biochem. 2012;48:28–38. doi: 10.1016/j.soilbio.2012.01.011. DOI
Tuor U., Winterhalter K., Fiechter A. Enzymes of White-Rot Fungi Involved in Lignin Degradation and Ecological Determinants for Wood Decay. J. Biotechnol. 1995;41:1–17. doi: 10.1016/0168-1656(95)00042-O. DOI
Baldrian P., Šnajdr J., Merhautová V., Dobiášová P., Cajthaml T., Valášková V. Responses of the Extracellular Enzyme Activities in Hardwood Forest to Soil Temperature and Seasonality and the Potential Effects of Climate Change. Soil Biol. Biochem. 2013;56:60–68. doi: 10.1016/j.soilbio.2012.01.020. DOI
Criquet S., Farnet A.M., Tagger S., Le Petit J. Annual Variations of Phenoloxidase Activities in an Evergreen Oak Litter: Influence of Certain Biotic and Abiotic Factors. Soil Biol. Biochem. 2000;32:1505–1513. doi: 10.1016/S0038-0717(00)00027-4. DOI
Sardans J., Peñuelas J. Drought Decreases Soil Enzyme Activity in a Mediterranean Quercus ilex L. Forest. Soil Biol. Biochem. 2005;37:455–461. doi: 10.1016/j.soilbio.2004.08.004. DOI
Baldrian P., Merhautová V., Cajthaml T., Petránková M., Šnajdr J. Small-Scale Distribution of Extracellular Enzymes, Fungal, and Bacterial Biomass in Quercus Petraea Forest Topsoil. Biol. Fertil. Soils. 2010;46:717–726. doi: 10.1007/s00374-010-0478-4. DOI
Crowther T.W., Jones T.H., Boddy L., Baldrian P. Invertebrate Grazing Determines Enzyme Production by Basidiomycete Fungi. Soil Biol. Biochem. 2011;43:2060–2068. doi: 10.1016/j.soilbio.2011.06.003. DOI
Hiscox J., Baldrian P., Rogers H.J., Boddy L. Changes in Oxidative Enzyme Activity during Interspecific Mycelial Interactions Involving the White-Rot Fungus Trametes Versicolor. Fungal Genet. Biol. 2010;47:562–571. doi: 10.1016/j.fgb.2010.03.007. PubMed DOI
Šnajdr J., Dobiášová P., Větrovský T., Valášková V., Alawi A., Boddy L., Baldrian P. Saprotrophic Basidiomycete Mycelia and Their Interspecific Interactions Affect the Spatial Distribution of Extracellular Enzymes in Soil. FEMS Microbiol. Ecol. 2011;78:80–90. doi: 10.1111/j.1574-6941.2011.01123.x. PubMed DOI
Lustenhouwer N., Maynard D.S., Bradford M.A., Lindner D.L., Oberle B., Zanne A.E., Crowther T.W. A Trait-Based Understanding of Wood Decomposition by Fungi. Proc. Natl. Acad. Sci. USA. 2020;117:11551–11558. doi: 10.1073/pnas.1909166117. PubMed DOI PMC
Anderson-Teixeira K.J., Davies S.J., Bennett A.C., Gonzalez-Akre E.B., Muller-Landau H.C., Joseph Wright S., Abu Salim K., Almeyda Zambrano M., Alonso A., Baltzer J.L., et al. CTFS-ForestGEO: A Worldwide Network Monitoring Forests in an Era of Global Change. Glob. Chang. Biol. 2015;21:528–549. doi: 10.1111/gcb.12712. PubMed DOI
Davies S.J., Abiem I., Abu Salim K., Aguilar S., Allen D., Alonso A., Anderson-Teixeira K., Andrade A., Arellano G., Ashton P.S., et al. ForestGEO: Understanding Forest Diversity and Dynamics through a Global Observatory Network. Biol. Conserv. 2021;253:108907. doi: 10.1016/j.biocon.2020.108907. DOI
Baldrian P., Zrůstová P., Tláskal V., Davidová A., Merhautová V., Vrška T. Fungi Associated with Decomposing Deadwood in a Natural Beech-Dominated Forest. Fungal Ecol. 2016;23:109–122. doi: 10.1016/j.funeco.2016.07.001. DOI
King H.G.C., Heath G.W. The Chemical Analysis of Small Samples Leaf Material and the Relationship between the Disappearance and Composition of Leaves. Pedobiologia. 1967;7:192–197.
DuBois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. 1956;28:350–356. doi: 10.1021/ac60111a017. DOI
Ihrmark K., Bödeker I.T.M., Cruz-Martinez K., Friberg H., Kubartova A., Schenck J., Strid Y., Stenlid J., Brandström-Durling M., Clemmensen K.E., et al. 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
Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Lozupone C.A., Turnbaugh P.J., Fierer N., Knight R. Global Patterns of 16S RRNA Diversity at a Depth of Millions of Sequences per Sample. Proc. Natl. Acad. Sci. USA. 2011;108((Suppl. 1)):4516–4522. doi: 10.1073/pnas.1000080107. 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
Chemidlin Prévost-Bouré N., Christen R., Dequiedt S., Mougel C., Lelièvre M., Jolivet C., Shahbazkia H.R., Guillou L., Arrouays D., Ranjard L. Validation and Application of a PCR Primer Set to Quantify Fungal Communities in the Soil Environment by Real-Time Quantitative PCR. PLoS ONE. 2011;6:e24166. doi: 10.1371/journal.pone.0024166. PubMed DOI PMC
Amann R.I., Ludwig W., Schleifer K.H. Phylogenetic Identification and in Situ Detection of Individual Microbial Cells without Cultivation. Microbiol. Rev. 1995;59:143–169. doi: 10.1128/mr.59.1.143-169.1995. PubMed DOI PMC
Wilmotte A., Van der Auwera G., De Wachter R. Structure of the 16 S Ribosomal RNA of the Thermophilic Cyanobacterium Chlorogloeopsis HTF (‘mastigocladus laminosus HTF’) Strain PCC7518, and Phylogenetic Analysis. FEBS Lett. 1993;317:96–100. doi: 10.1016/0014-5793(93)81499-P. PubMed DOI
Větrovský T., Baldrian P., Morais D. SEED 2: A User-Friendly Platform for Amplicon High-Throughput Sequencing Data Analyses. Bioinformatics. 2018;34:2292–2294. doi: 10.1093/bioinformatics/bty071. PubMed DOI PMC
Aronesty E. Comparison of Sequencing Utility Programs. Open Bioinforma. J. 2013;7:1–8. doi: 10.2174/1875036201307010001. DOI
Nilsson R.H., 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 R.C. Search and Clustering Orders of Magnitude Faster than BLAST. Bioinformatics. 2010;26:2460–2461. doi: 10.1093/bioinformatics/btq461. PubMed DOI
Edgar R.C. UPARSE: Highly Accurate OTU Sequences from Microbial Amplicon Reads. Nat. Methods. 2013;10:996–998. doi: 10.1038/nmeth.2604. PubMed DOI
Kõljalg U., Nilsson R.H., Abarenkov K., Tedersoo L., Taylor A.F.S., Bahram M., Bates S.T., Bruns T.D., Bengtsson-Palme J., Callaghan T.M., et al. Towards a Unified Paradigm for Sequence-Based Identification of Fungi. Mol. Ecol. 2013;22:5271–5277. doi: 10.1111/mec.12481. PubMed DOI
Põlme S., Abarenkov K., Nilsson R.H., Lindahl B.D., Clemmensen K.E., Kauserud H., Nguyen N., Kjøller R., Bates S.T., Baldrian P., et al. FungalTraits: A User-Friendly Traits Database of Fungi and Fungus-like Stramenopiles. Fungal Divers. 2020;105:1–16. doi: 10.1007/s13225-020-00466-2. DOI
R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2020.
Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., McGlinn D., Minchin P.R., O’Hara R.B., Simpson G.L., Solymos P., et al. Package “Vegan” Version 2.5-7. [(accessed on 20 January 2020)]. Available online: https://cran.r-project.org/web/packages/vegan/vegan.pdf.
Rosseel Y. Lavaan: An R Package for Structural Equation Modeling. Stat. Softw. 2012;48:1–36. doi: 10.18637/jss.v048.i02. DOI
Baldrian P., Merhautová V., Petránková M., Cajthaml T., Šnajdr J. Distribution of Microbial Biomass and Activity of Extracellular Enzymes in a Hardwood Forest Soil Reflect Soil Moisture Content. Appl. Soil Ecol. 2010;46:177–182. doi: 10.1016/j.apsoil.2010.08.013. DOI
Criquet S., Tagger S., Vogt G., Le Petit J. Endoglucanase and β-Glycosidase Activities in an Evergreen Oak Litter: Annual Variation and Regulating Factors. Soil Biol. Biochem. 2002;34:1111–1120. doi: 10.1016/S0038-0717(02)00045-7. DOI
Criquet S., Ferre E., Farnet A.M., Le Petit J. Annual Dynamics of Phosphatase Activities in an Evergreen Oak Litter: Influence of Biotic and Abiotic Factors. Soil Biol. Biochem. 2004;36:1111–1118. doi: 10.1016/j.soilbio.2004.02.021. DOI
Jomura M., Kominami Y., Dannoura M., Kanazawa Y. Spatial Variation in Respiration from Coarse Woody Debris in a Temperate Secondary Broad-Leaved Forest in Japan. For. Ecol. Manage. 2008;255:149–155. doi: 10.1016/j.foreco.2007.09.002. DOI
Vermaas J.V., Petridis L., Qi X., Schulz R., Lindner B., Smith J.C. Mechanism of Lignin Inhibition of Enzymatic Biomass Deconstruction. Biotechnol. Biofuels. 2015;8:217. doi: 10.1186/s13068-015-0379-8. PubMed DOI PMC
Fukasawa Y., Osono T., Takeda H. Dynamics of Physicochemical Properties and Occurrence of Fungal Fruit Bodies during Decomposition of Coarse Woody Debris of Fagus Crenata. J. For. Res. 2009;14:20–29. doi: 10.1007/s10310-008-0098-0. DOI
Rajala T., Peltoniemi M., Pennanen T., Mäkipää R. Relationship between Wood-Inhabiting Fungi Determined by Molecular Analysis (Denaturing Gradient Gel Electrophoresis) and Quality of Decaying Logs. Can. J. For. Res. 2010;40:2384–2397. doi: 10.1139/X10-176. DOI
Swift M.J., Heal O.W., Anderson J.M. Decomposition in Terrestrial Ecosystems. University of California Press; Berkeley, CA, USA: 1979.
Lepinay C., Jiráska L., Tláskal V., Brabcová V., Vrška T., Baldrian P. Successional Development of Fungal Communities Associated with Decomposing Deadwood in a Natural Mixed Temperate Forest. J. Fungi. 2021;7:412. doi: 10.3390/jof7060412. PubMed DOI PMC