Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29491492
PubMed Central
PMC6018761
DOI
10.1038/s41396-018-0084-2
PII: 10.1038/s41396-018-0084-2
Knihovny.cz E-zdroje
- MeSH
- Bacteria klasifikace genetika izolace a purifikace metabolismus MeSH
- biodegradace MeSH
- biomasa MeSH
- ekosystém MeSH
- houby klasifikace genetika izolace a purifikace metabolismus MeSH
- lesy MeSH
- půda chemie MeSH
- půdní mikrobiologie * MeSH
- rostliny metabolismus mikrobiologie MeSH
- uhlík metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- půda MeSH
- uhlík MeSH
Forest soils represent important terrestrial carbon (C) pools where C is primarily fixed in the plant-derived biomass but it flows further through the biomass of fungi and bacteria before it is lost from the ecosystem as CO2 or immobilized in recalcitrant organic matter. Microorganisms are the main drivers of C flow in forests and play critical roles in the C balance through the decomposition of dead biomass of different origins. Here, we track the path of C that enters forest soil by following respiration, microbial biomass production, and C accumulation by individual microbial taxa in soil microcosms upon the addition of 13C-labeled biomass of plant, fungal, and bacterial origin. We demonstrate that both fungi and bacteria are involved in the assimilation and mineralization of C from the major complex sources existing in soil. Decomposer fungi are, however, better suited to utilize plant biomass compounds, whereas the ability to utilize fungal and bacterial biomass is more frequent among bacteria. Due to the ability of microorganisms to recycle microbial biomass, we suggest that the decomposer food web in forest soil displays a network structure with loops between and within individual pools. These results question the present paradigms describing food webs as hierarchical structures with unidirectional flow of C and assumptions about the dominance of fungi in the decomposition of complex organic matter.
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Lladó S, López-Mondéjar R, Baldrian P. Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol Rev. 2017;81:e00063–16. doi: 10.1128/MMBR.00063-16. PubMed DOI PMC
Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, et al. A large and persistent carbon sink in the world’s forests. Science. 2011;333:988–93. doi: 10.1126/science.1201609. PubMed DOI
Baldrian P. Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev. 2017;41:109–30. PubMed
Schimel JP, Schaeffer SM. Microbial control over carbon cycling in soil. Front Microbiol. 2012;3:348. doi: 10.3389/fmicb.2012.00348. PubMed DOI PMC
de Vries FT, Thébault E, Liiri M, Birkhofe K, Tsiafouli MA, Bjørnlund L, et al. Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci USA. 2013;110:14296–301. doi: 10.1073/pnas.1305198110. PubMed DOI PMC
Rousk J, Frey SD. Revisiting the hypothesis that fungal-to-bacterial dominance characterises turnover of soil organic matter and nutrients. Ecol Monogr. 2015;85:457–72. doi: 10.1890/14-1796.1. DOI
Xia M, Talhelm AF, Pregitzer KS. Fine roots are the dominant source of recalcitrant plant litter in sugar maple-dominated northern hardwood forests. New Phytol. 2015;208:715–26. doi: 10.1111/nph.13494. PubMed DOI PMC
Voříšková J, Brabcová V, Cajthaml T, Baldrian P. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol. 2014;201:269–78. doi: 10.1111/nph.12481. PubMed DOI
Eichlerová I, Homolka L, Žifčáková L, Lisá L, Dobiášová P, Baldrian P. Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi. Fungal Ecol. 2015;13:10–22. doi: 10.1016/j.funeco.2014.08.002. DOI
Sterkenburg E, Bahr A, Brandstrom Durling M, Clemmensen KE, Lindahl BD. Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol. 2015;207:1145–58. doi: 10.1111/nph.13426. PubMed DOI
van der Wal A, Geydan TD, Kuyper TW, de Boer W. A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev. 2013;37:477–94. doi: 10.1111/1574-6976.12001. PubMed DOI
López-Mondéjar R, Zuhlke D, Becher D, Riedel K, Baldrian P. Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep. 2016;6:25279. doi: 10.1038/srep25279. PubMed DOI PMC
Berlemont R, Martiny AC. Genomic potential for polysaccharides deconstruction in bacteria. Appl Environ Microbiol. 2015;81:1513–9. doi: 10.1128/AEM.03718-14. PubMed DOI PMC
Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P. Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol. 2012;80:735–46. doi: 10.1111/j.1574-6941.2012.01343.x. PubMed DOI
Esperschütz J, Pérez-de-Mora A, Schreiner K, Welzl G, Buegger F, Zeyer J, et al. Microbial food web dynamics along a soil chronosequence of a glacier forefield. Biogeosciences. 2011;8:3283–94. doi: 10.5194/bg-8-3283-2011. DOI
Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P, et al. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil. 2013;366:1–27. doi: 10.1007/s11104-013-1630-3. DOI
Brabcová V, Nováková M, Davidová A, Baldrian P. Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytol. 2016;210:1369–81. doi: 10.1111/nph.13849. PubMed DOI
Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, et al. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J. 2012;6:248–58. doi: 10.1038/ismej.2011.95. PubMed DOI PMC
Gunina A, Dippold M, Glaser B, Kuzyakov Y. Turnover of microbial groups and cell components in soil: 13C analysis of cellular biomarkers. Biogeosciences. 2017;14:271–83. doi: 10.5194/bg-14-271-2017. DOI
Wang X, Sharp CE, Jones GM, Grasby SE, Brady AL, Dunfield PF. Stable-isotope probing identifies uncultured planctomycetes as primary degraders of a complex heteropolysaccharide in soil. Appl Environ Microbiol. 2015;81:4607–15. doi: 10.1128/AEM.00055-15. PubMed DOI PMC
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. doi: 10.1016/j.soilbio.2017.12.012. DOI
de Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29:795–811. doi: 10.1016/j.femsre.2004.11.005. PubMed DOI
Fierer N, Bradford MA, Jackson R. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–64. doi: 10.1890/05-1839. PubMed DOI
Lladó S, Žifčáková L, Větrovský T, Eichlerová I, Baldrian P. Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol Fertil Soils. 2015;52:251–60. doi: 10.1007/s00374-015-1072-6. DOI
Morrissey EM, Mau RL, Schwartz E, Caporaso JG, Dijkstra P, van Gestel N, et al. Phylogenetic organization of bacterial activity. ISME J. 2016;10:2336–40. doi: 10.1038/ismej.2016.28. PubMed DOI PMC
Trivedi P, Anderson IC, Singh BK. Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol. 2013;21:641–51. doi: 10.1016/j.tim.2013.09.005. PubMed DOI
Kramer S, Dibbern D, Moll J, Huenninghaus M, Koller R, Krueger D, et al. Resource partitioning between bacteria, fungi, and protists in the detritusphere of an agricultural soil. Front Microbiol. 2016;7:1524. doi: 10.3389/fmicb.2016.01524. PubMed DOI PMC
Mariadassou M, Pichon S, Ebert D. Microbial ecosystems are dominated by specialist taxa. Ecol Lett. 2015;18:974–82. doi: 10.1111/ele.12478. PubMed DOI
Urbanová M, Šnajdr J, Baldrian P. Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol Biochem. 2015;84:53–64. doi: 10.1016/j.soilbio.2015.02.011. DOI
Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P. Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem. 2008;40:2068–75. doi: 10.1016/j.soilbio.2008.01.015. 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;46:717–26. doi: 10.1007/s00374-010-0478-4. 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
López-Mondéjar R, Voříšková J, Větrovský T, Baldrian P. The bacterial community inhabiting temperate deciduous forests is vertically stratified and undergoes seasonal dynamics. Soil Biol Biochem. 2015;87:43–50. doi: 10.1016/j.soilbio.2015.04.008. DOI
Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911–7. doi: 10.1139/y59-099. PubMed DOI
Ihrmark K, Bodeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, et al. New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol. 2012;82:666–77. doi: 10.1111/j.1574-6941.2012.01437.x. PubMed DOI
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4. doi: 10.1038/ismej.2012.8. 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
Větrovský T, Baldrian P. Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils. 2013;49:1027–37. doi: 10.1007/s00374-013-0801-y. DOI
Cole JR, Wang Q, Fish JA, Chai BL, McGarrell DM, Sun YN, et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42:D633–D642. doi: 10.1093/nar/gkt1244. PubMed DOI PMC
Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–7. doi: 10.1111/mec.12481. PubMed DOI
Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, et al. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinforma. 2008;9:386. doi: 10.1186/1471-2105-9-386. PubMed DOI PMC
Verastegui Y, Cheng J, Engel K, Kolczynski D, Mortimer S, Lavigne J, et al. Multisubstrate isotope labeling and metagenomic analysis of active soil bacterial communities. mBio. 2014;5:e01157–01114. doi: 10.1128/mBio.01157-14. PubMed DOI PMC
Bode S, Fancy R, Boeckx P. Stable isotope probing of amino sugars--a promising tool to assess microbial interactions in soils. Rapid Comm Mass Spectrom. 2013;27:1367–79. doi: 10.1002/rcm.6586. PubMed DOI
Chen Y, Murrell JC. When metagenomics meets stable-isotope probing: progress and perspectives. Trends Microbiol. 2010;18:157–63. doi: 10.1016/j.tim.2010.02.002. PubMed DOI
Větrovský T, Steffen KT, Baldrian P. Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil actinobacteria. PLoS ONE. 2014;9:e89108. doi: 10.1371/journal.pone.0089108. PubMed DOI PMC
Dedysh SN. Cultivating uncultured bacteria from northern wetlands: knowledge gained and remaining gaps. Front Microbiol. 2011;2:15. doi: 10.3389/fmicb.2011.00184. PubMed DOI PMC
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, et al. Roots and associated fungi drive long-term carbon sequestration in boreal. For Sci. 2013;339:1615–8. doi: 10.1126/science.1231923. PubMed DOI
Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal PK, Wu S, et al. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol. 2017;19:2964–83. doi: 10.1111/1462-2920.13669. PubMed DOI
Phillips LA, Ward V, Jones MD. Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J. 2014;8:699–713. doi: 10.1038/ismej.2013.195. PubMed DOI PMC
Zeng J, Zheng Y, Yu X, Yu L, Gao D, Chen S. Lignocellulosic biomass as a carbohydrate source for lipid production by Mortierella isabellina. Biores Technol. 2013;128:385–91. doi: 10.1016/j.biortech.2012.10.079. PubMed DOI
Fuentes S, Barra B, Caporaso JG, Seeger M. From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation. Appl Environ Microbiol. 2015;82:888–96. doi: 10.1128/AEM.02625-15. PubMed DOI PMC
Kim SJ, Park SJ, Jung MY, Kim JG, Madsen EL, Rhee SK. An uncultivated nitrate-reducing member of the genus Herminiimonas degrades toluene. Appl Environ Microbiol. 2014;80:3233–43. doi: 10.1128/AEM.03975-13. PubMed DOI PMC
Krizova L, Maixnerova M, Sedo O, Nemec A. Acinetobacter bohemicus sp. nov. widespread in natural soil and water ecosystems in the Czech Republic. Syst Appl Microbiol. 2014;37:467–73. doi: 10.1016/j.syapm.2014.07.001. PubMed DOI
Shashkov AS, Streshinskaya GM, Tul’skaya EM, Senchenkova SN, Baryshnikova LM, Dmitrenok AS, et al. Cell wall glycopolymers of Streptomyces albus, Streptomyces albidoflavus and Streptomyces pathocidini. Anton Leeuw. 2016;109:923–36. doi: 10.1007/s10482-016-0691-8. PubMed DOI
Lueders T, Kindler R, Miltner A, Friedrich MW, Kaestner M. Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl Environ Microbiol. 2006;72:5342–8. doi: 10.1128/AEM.00400-06. PubMed DOI PMC
Mašínová T, Bahnmann BD, Větrovský T, Tomšovský M, Merunková K, Baldrian P. Drivers of yeast community composition in the litter and soil of a temperate forest. FEMS Microbiol Ecol. 2017;93:fiw223. doi: 10.1093/femsec/fiw223. PubMed DOI
Koch AL. Oligotrophs versus copiotrophs. BioEssays. 2001;23:657–61. doi: 10.1002/bies.1091. PubMed DOI
Lladó S, Baldrian P. Community-level physiological profiling analyses show potential to identify the copiotrophic bacteria present in soil environments. PLoS ONE. 2017;12:e0171638. doi: 10.1371/journal.pone.0171638. PubMed DOI PMC
Kurm V, Van der Putten WH, De Boer W, Naus-Wiezer S, Hol WHG. Low abundant soil bacteria can be metabolically versatile and fast growing. Ecology. 2017;98:555–64. doi: 10.1002/ecy.1670. PubMed DOI
Pepe-Ranney C, Campbell AN, Koechli CN, Berthrong S, Buckley DH. Unearthing the ecology of soil microorganisms using a high resolution DNA-SIP approach to explore cellulose and xylose metabolism in soil. Front Microbiol. 2016;7:703. doi: 10.3389/fmicb.2016.00703. PubMed DOI PMC
Tláskal V, Voříšková J, Baldrian P. Bacterial succession on decomposing leaf litter exhibits a specific occurrence pattern of cellulolytic taxa and potential decomposers of fungal mycelia. FEMS Microbiol Ecol. 2016;92:fiw177. doi: 10.1093/femsec/fiw177. PubMed DOI
Crowther TW, Stanton DWG, Thomas SM, A’Bear AD, Hiscox J, Jones TH, et al. Top-down control of soil fungal community composition by a globally distributed keystone consumer. Ecology. 2013;94:2518–28. doi: 10.1890/13-0197.1. PubMed DOI
Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, et al. Soil invertebrates disrupt carbon flow through fungal networks. Science. 2005;309:1047–1047. doi: 10.1126/science.1114769. PubMed DOI
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