Decomposition of peatland DOC affected by root exudates is driven by specific r and K strategic bacterial taxa

. 2021 Sep 21 ; 11 (1) : 18677. [epub] 20210921

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34548501
Odkazy

PubMed 34548501
PubMed Central PMC8455546
DOI 10.1038/s41598-021-97698-2
PII: 10.1038/s41598-021-97698-2
Knihovny.cz E-zdroje

In peatlands, decomposition of organic matter is limited by harsh environmental conditions and low decomposability of the plant material. Shifting vegetation composition from Sphagnum towards vascular plants is expected in response to climate change, which will lead to increased root exudate flux to the soil and stimulation of microbial growth and activity. We aimed to evaluate the effect of root exudates on the decomposition of recalcitrant dissolved organic carbon (DOC) and to identify microorganisms involved in this process. The exudation was mimicked by an addition of a mixture of 13C labelled compounds into the recalcitrant DOC in two realistic levels; 2% and 5% of total DOC and peatland porewater with added root exudates was incubated under controlled conditions in the lab. The early stage of incubation was characterized by a relative increase of r-strategic bacteria mainly from Gammaproteobacteria and Bacteriodetes phyla within the microbial community and their preferential use of the added compounds. At the later stage, Alphaproteobacteria and Acidobacteria members were the dominating phyla, which metabolized both the transformed 13C compounds and the recalcitrant DOC. Only higher exudate input (5% of total DOC) stimulated decomposition of recalcitrant DOC compared to non-amended control. The most important taxa with a potential to decompose complex DOC compounds were identified as: Mucilaginibacter (Bacteriodetes), Burkholderia and Pseudomonas (Gammaproteobacteria) among r-strategists and Bryocella and Candidatus Solibacter (Acidobacteria) among K-strategists. We conclude that increased root exudate inputs and their increasing C/N ratio stimulate growth and degradation potential of both r-strategic and K-strategic bacteria, which make the system more dynamic and may accelerate decomposition of peatland recalcitrant DOC.

Zobrazit více v PubMed

Tfaily MM, et al. Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques. Geochim. Cosmochim. Acta. 2013;112:116–129. doi: 10.1016/j.gca.2013.03.002. DOI

Thacker SA, et al. Functional properties of DOM in a stream draining peat. Sci. Total Environ. 2008;407:566–573. doi: 10.1016/j.scitotenv.2008.09.011. PubMed DOI

Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: Carbon trading at the soil-root interface. Plant Soil. 2009;321:5–33. doi: 10.1007/s11104-009-9925-0. DOI

Shackle VJ, Freeman C, Reynolds B. Carbon supply and the regulation of enzyme activity in constructed wetlands. Soil Biol. Biochem. 2000;32(13):1935–1940. doi: 10.1016/S0038-0717(00)00169-3. DOI

van Huissteden J, van den Bos R, Alvarez IM. Modelling the effect of watertable management on CO2 and CH4 fluxes from peat soils. Neth. J. Geosci. Geol. Mijnbouw. 2006;85:3–18. doi: 10.1017/S0016774600021399. DOI

Hamer U, Marschner B. Priming effects of sugars, amino acids, organic acids and catechol on the mineralization of lignin and peat. GJSSPN Z. Pflanzenernahr. Bodenkd. 2002;165:261–268. doi: 10.1002/1522-2624(200206)165:3<261::AID-JPLN261>3.0.CO;2-I. DOI

Basiliko N, et al. Do root exudates enhance peat decomposition? Geomicrobiol. J. 2012;29:374–378. doi: 10.1080/01490451.2011.568272. DOI

Dieleman CM, et al. Climate change drives a shift in peatland ecosystem plant community: Implications for ecosystem function and stability. Global Change Biol. 2015;21:388–395. doi: 10.1111/gcb.12643. PubMed DOI

Frolking S, et al. Modelling seasonal to annual carbon balance of Mer Bleue Bog, Ontario, Canada. Global Biogeochem. Cycles. 2002;16:1029–1040.

Zhu B, et al. Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol. Biochem. 2014;76:183–192. doi: 10.1016/j.soilbio.2014.04.033. DOI

Hotchkiss ER, et al. Modeling priming effects on microbial consumption of dissolved organic carbon in rivers. J. Geophys. Res. Biogeosci. 2014;119:982–995. doi: 10.1002/2013JG002599. DOI

Liu X-JA, et al. Labile carbon input determines the direction and magnitude of the priming effect. Appl. Soil Ecol. 2017;109:7–13. doi: 10.1016/j.apsoil.2016.10.002. DOI

Shi S, et al. Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol. Ecol. 2011;77:600–610. doi: 10.1111/j.1574-6941.2011.01150.x. PubMed DOI

Grayston SJ, Vaughan D, Jones D. Rhizosphere carbon flow in trees, in comparison with annual plants: The importance of root exudation and its impact on microbial activity and nutrient availability. Appl. Soil Ecol. 1997;5:29–56. doi: 10.1016/S0929-1393(96)00126-6. DOI

Chen R, et al. Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Global Change Biol. 2014;20:2356–2367. doi: 10.1111/gcb.12475. PubMed DOI

Qiao N, et al. Carbon and nitrogen additions induce distinct priming effects along an organic-matter decay continuum. Sci. Rep. 2016;6:1–8. doi: 10.1038/s41598-016-0001-8. PubMed DOI PMC

Fontaine S, et al. Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol. Biochem. 2011;43:86–96. doi: 10.1016/j.soilbio.2010.09.017. DOI

Edwards KR, et al. Species effects and seasonal trends on plant efflux quantity and quality in a spruce swamp forest. Plant Soil. 2018;426:179–196. doi: 10.1007/s11104-018-3610-0. DOI

Andrews JH, Harris RF. r- and K-selection and microbial ecology. Adv. Microb. Ecol. 1986;9:99–147. doi: 10.1007/978-1-4757-0611-6_3. DOI

Kuzyakov Y. Priming effects: Interactions between living and dead organic matter. Soil Biol. Biochem. 2010;42:1363–1371. doi: 10.1016/j.soilbio.2010.04.003. DOI

Wild B, et al. Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil. Soil Biol. Biochem. 2014;75:143–151. doi: 10.1016/j.soilbio.2014.04.014. PubMed DOI PMC

Schimel JP, Schaeffer SM. Microbial control over carbon cycling in soil. Front. Microbiol. 2012;3(348):1–11. PubMed PMC

Blagodatskaya E, et al. Microbial interactions affect sources of priming induced by cellulose. Soil Biol. Biochem. 2014;74:39–49. doi: 10.1016/j.soilbio.2014.02.017. DOI

Garcia-Pausas J, Paterson E. Microbial community abundance and structure are determinants of soil organic matter mineralisation in the presence of labile carbon. Soil Biol. Biochem. 2011;43:1705–1715. doi: 10.1016/j.soilbio.2011.04.016. DOI

Myers B, et al. Microbial activity across a boreal peatland nutrient gradient: The role of fungi and bacteria. Wetl. Ecol. Manag. 2012;20:77–88. doi: 10.1007/s11273-011-9242-2. DOI

Chroňáková A, et al. Spatial heterogeneity of belowground microbial communities linked to peatland microhabitats with different plant dominants. FEMS Microbiol. Ecol. 2019;95(9):fiz13. doi: 10.1093/femsec/fiz130. PubMed DOI PMC

Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–1364. doi: 10.1890/05-1839. PubMed DOI

Painter TJ. Lindow man, Tollund man and other peat-bog bodies—The preservative and antimicrobial action of sphagnan, a reactive glycuronoglycan with tanning and sequestering properties. Carbohydr. Polym. 1991;15:123–142. doi: 10.1016/0144-8617(91)90028-B. DOI

Wang H, et al. Quality offresh organic matter affects priming of soil organic matter and substrate utili-zation patterns of microbes. Sci. Rep. 2015;5:10102. doi: 10.1038/srep10102. PubMed DOI PMC

Jenkins SN, et al. Taxon-specific responses of soil bacteria to the addition of low level C inputs. Soil Biol. Biochem. 2010;42:1624–1631. doi: 10.1016/j.soilbio.2010.06.002. DOI

Lladó S, et al. Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol. Fertil. Soils. 2016;52:251–260. doi: 10.1007/s00374-015-1072-6. DOI

Rodriguez H, Fraga R. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 1999;17:319–339. doi: 10.1016/S0734-9750(99)00014-2. PubMed DOI

Pankratov TA, et al. Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat. Environ. Microbiol. 2011;13:1800–1814. doi: 10.1111/j.1462-2920.2011.02491.x. PubMed DOI

Kaštovská E, et al. Cotton-grass and blueberry have opposite effect on peat characteristics and nutrient transformation in peatland. Ecosystems. 2018;21:443–458. doi: 10.1007/s10021-017-0159-3. DOI

Mastný J, et al. Quality of DOC produced during litter decomposition of peatland plant dominants. Soil Biol. Biochem. 2018;121:221–230. doi: 10.1016/j.soilbio.2018.03.018. DOI

Drake JE, et al. Stoichiometry constrains microbial response to root exudation—Insights from a model and a field experiment in a temperate forest. Biogeosciences. 2013;10:821–838. doi: 10.5194/bg-10-821-2013. DOI

Urich T, et al. Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE. 2008;3:e2527. doi: 10.1371/journal.pone.0002527. PubMed DOI PMC

Caporaso JG, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U. S. A. 2010;108(Suppl 1):4516–4522. PubMed PMC

Gardes M, Bruns TD. Its primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993;2:113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x. PubMed DOI

Edgar RC, Robert C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Br. J. Pharmacol. 2013;10:996–998. PubMed

Bengtsson-Palme J, et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 2013;4:914–919.

Quast C, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

Kõljalg U, 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

Muyzer G, Dewaal EC, Uitterlinden AG. Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16s ribosomal-Rna. Appl. Environ. Microbiol. 1993;59:695–700. doi: 10.1128/aem.59.3.695-700.1993. PubMed DOI PMC

Borneman J, Hartin RJ. PCR primers that amplify fungal rRNA genes from environmental samples. Appl. Environ. Microbiol. 2000;66:4356–4360. doi: 10.1128/AEM.66.10.4356-4360.2000. PubMed DOI PMC

Langille M, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013;31:814–821. doi: 10.1038/nbt.2676. PubMed DOI PMC

Louca S, Parfrey LW, Doebel M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353:1272–1277. doi: 10.1126/science.aaf4507. PubMed DOI

Thompson LR, et al. A communal catalogue reveals Earth's multiscale microbial diversity. Nature. 2017;551:457–463. doi: 10.1038/nature24621. PubMed DOI PMC

Parks DH, et al. STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–3124. doi: 10.1093/bioinformatics/btu494. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace