Multiple environmental factors, but not nutrient addition, directly affect wet grassland soil microbial community structure: a mesocosm study

. 2023 Jun 16 ; 99 (7) : .

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37355783

Nutrient addition may change soil microbial community structure, but soil microbes must simultaneously contend with other, interacting factors. We studied the effect of soil type (peat, mineral), water level (low, high), and nutrient addition (unfertilized, fertilized) on wet grassland soil microbial community structure in both vegetated and un-vegetated soils after five years of treatment application in a mesocosm, using Illumina sequencing of the bacterial V4 region of the small ribosomal sub-units. Soil type, water level, and plant presence significantly affected the soil microbial structure, both singly and interactively. Nutrient addition did not directly impact microbiome structure, but acted indirectly by increasing plant biomass. The abundance of possible plant growth promoting bacteria and heterotrophic bacteria indicates the importance of bacteria that promote plant growth. Based on our results, a drier and warmer future would result in nutrient-richer conditions and changes to microbial community structure and total microbial biomass and/or abundances, with wet grasslands likely switching from areas acting as C sinks to C sources.

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Akaike H. Factor analysis and AIC. Psychometrika. 1987;52:317–32.

Aronesty E. Comparison of sequencing utility programs. Open Bioinform J. 2013;7:1–8.

Bárta J, Tahovská K, Šantrůčková Het al. . Microbial communities with distinct denitrification potential in spruce and beech soils differing in nitrate leaching. Sci Rep. 2017;7:9738, doi.org/10.1038/s41598-017-08554-1. PubMed PMC

Bates ST, Berg-Lyons D, Caporaso JGet al. . Examining the global distribution of dominant archaeal populations in soil. ISME J. 2011;5:908–17. PubMed PMC

Bennett AE, Evans DM, Powell JR. Potentials and pitfalls in the analysis of bipartite networks to understand plant-microbe interactions in changing environments. Funct Ecol. 2018;33:107–17.

Berg G, Smalla K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol. 2009;68:1–13. PubMed

Borneman J, Hartin RJ. PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microbiol. 2000;66:4356–60., doi: 10.1128/aem.66.10.4356-4360.2000. PubMed PMC

Buyer JS, Kaufman DD. Microbial diversity in the rhizosphere of corn grown under conventional and low-input systems. Appl Soil Ecol. 1996;5:21–7.

Cao Y, Ma C, Chen Het al. . Copper stress in flooded soil: impact on enzyme activities, microbial community composition and diversity in the rhizosphere of Salix integra. Sci Total Environ. 2020;704:135350. 10.1016/j.scitotenv.2019.135350. PubMed DOI

Caporaso JG, Kuczynski J, Stombaugh Jet al. . QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6. PubMed PMC

Caporaso JG, Lauber CL, Walter WAet al. . Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108:4516–22., doi: 10.1073/pnas.1000080107. PubMed PMC

Carey CJ, Dove NC, Beman JMet al. . Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem. 2016;99:158–66.

Cheng Y, Wang J, Wang Jet al. . Nitrogen deposition differentially affects soil gross nitrogen transformations in organic and mineral horizons. Earth Sci Rev. 2020;201:103033. 10.1016/j.earscirev.2019.103033. DOI

Chialva M, Ghignone S, Cozzi Pet al. . Water management and phenology influence the root-associated rice field microbiota. FEMS Microbiol Ecol. 2020;96:fiaa146. 10.1093/femsec/fiaa146. PubMed DOI

Chroňáková A, Bárta J, Kaštovská Eet al. . Spatial heterogeneity of belowground microbial communities linked to peatland microhabitats with different plant dominants. FEMS Microbiol Ecol. 2019;95:fiz130. 10.1093/femsec/fiz130. PubMed DOI PMC

Colmer TD. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ. 2003;26:17–36.

Crecchio C, Curci M, Mininni Ret al. . Short-term effects of municipal solid waste compost amendments on soil carbon and nitrogen content, some enzyme activities and genetic diversity. Biol Fert Soils. 2001;34:311–8.

Delgado-Baquerizo M, Oliverio AM, Brewer TEet al. . A global atlas of the dominant bacteria found in soil. Science. 2018;359:320–5. PubMed

DeLong JR, Fry EL, Veen GFet al. . Why are plant-soil feedbacks so unpredictable, and what to do about it?. Funct Ecol. 2019;33:118–28.

Edgar RC UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8. PubMed

Edwards KR. Effect of nutrient additions and site hydrology on belowground production and root nutrient contents in two wet grasslands. Ecol Eng. 2015;84:325–35.

Edwards KR, Čížková H. Nutrient inputs and hydrology interact with plant functional type in affecting plant production and nutrient contents in a wet grassland. Wetlands. 2020;40:707–19.

Edwards KR, Picek T, Čížková Het al. . Nutrient addition effects on carbon fluxes in wet grasslands with either organic or mineral soil. Wetlands. 2015;35:55–68.

Ehrenfeld JG, Ravit B, Elgersma K. Feedback in the plant-soil system. Ann Rev Environ Res. 2005;30:75–115.

Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15: 579–90. PubMed

Fortney NW, He S, Converse BJet al. . Microbial Fe(III) oxide reduction potential in Chocolate Pots hot spring, Yellowstone National Park. Geobiology. 2016;14:255–75. PubMed

González OM, Steinauer K, Jousset Aet al. . Flood induced changes in soil microbial functions as modified by plant diversity. PLoS One. 2016;11:e0166349. PubMed PMC

Gutknecht JLM, Goodman RM, Balser TC. Linking soil process and microbial ecology in freshwater wetland ecosystems. Plant Soil. 2006;289:17–34.

Haichar FZ, Achouak W, Christen Ret al. . Identification of cellulytic bacteria in soil by stable isotope probing. Environ Microbiol. 2007;9:625–34. PubMed

Hansel CM, Fendorf S, Jardine PMet al. . Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol. 2008;74:1620–33. PubMed PMC

Hartman K, Tringe SG. Interactions between plants and soil shaping the root microbiome under abiotic stress. Biochem J. 2019;476:2705–24. PubMed PMC

Hawkes CV, DeAngelis KM, Firestone MK. Root interactions with soil microbial communities and processes. In: Cardon ZG, Whitbeck JL (eds.), The Rhizosphere. Amsterdam: Elsevier Academic Press, 2007, 1–29.

Hu SJ, Van Bruggen AHC, Grünwald NJ. Dynamics of bacterial populations in relation to carbon availability in a residue-amended soil. Appl Soil Ecol. 1999;13:21–30.

Iino T, Mori K, Uchino Yet al. . Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int J Syst Evol Microbiol. 2010;60:1376–82. PubMed

Jangid K, Williams MA, Franzleubbers AJet al. . Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem. 2008;40:2843–53.

Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil. 2009;321:5–33.

Joyce CB. Ecological consequences and restoration potential of abandoned wet grasslands. Ecol Eng. 2014;66:91–102. dx.doi.org/10.1016/j.ecoleng.2013.05.008. DOI

Joyce CB, Simpson M, Casanova M. Future wet grasslands: ecological implications of climate change. Ecosyst Health Sustain. 2016;2:e01240, doi.org/10.1002/ehs2.1240.

Joyce CB, Wade PM. European Wet Grasslands: Biodiversity, Management and Restoration. Chicester: Wiley, 1998.

Kielak AM, Barreto CC, Kowalchuk GAet al. . The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol. 2016;7:744. https://doi.org/10.3389/fmicb. 2016.00744. PubMed DOI PMC

Knief C. Diversity of methane-cycling microorganisms in soils and their relation to oxygen. Curr Issues Mol Biol. 2019;3:23–56. 10.21775/cimb.033.023. PubMed DOI

Kuramae EE, Yergeau E, Wong LCet al. . Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol. 2011;79:12–24. PubMed

Kuzyakov Y. Priming effects: interactions between living and dead organic matter. Soil Biol Biochem. 2010;42:1363–71.

Laanbroek HJ. Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Ann Bot. 2010;105:141–53. PubMed PMC

Lalonde K, Mucci A, Ouellet Aet al. . Preservation of organic matter in sediments promoted by iron. Nature. 2012;483:198–200. PubMed

Lamers LPM, van Diggelen JMH, Op den Camp HJMet al. . Microbial transformations of nitrogen, sulfur and iron dictate vegetation composition in wetlands: a review. Front Microbiol. 2012;3:156. 10.3389/fmicb.2012.00156. PubMed DOI PMC

Langille MGI, Zaneveld J, Caporaso JGet al. . Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814–21. PubMed PMC

Leininger S, Urich T, Schloteret al. . Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006;442:806–9. 10.1038/nature04983 PubMed DOI

Llado Fernandez S, Větrovský T, Baldrian P. The concept of operational taxonomic units revisited: genomes of bacteria that are regarded as closely related are often highly dissimilar. Folia Microbiol. 2019;64:19–23. PubMed

Lundberg DS, Lebeis SL, Paredes SHet al. . Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488:86–90. PubMed PMC

Luoto M, Pykälä J, Kuussaari M. Decline of landscape-scale habitat and species diversity after the end of cattle grazing. J Nat Conserv. 2003;11:171–8.

Maestre FT, Quero JL, Gotelli NJet al. . Plant species richness and ecosystem multifunctionality in global drylands. Science. 2012;335:214–8. PubMed PMC

Malik AA, Chowdhury S, Schlager Vet al. . Soil fungal: bacterial ratios are linked to altered carbon cycling. Front Microbiol. 2016;7:1247. 10.3389/fmicb.2016.01247. PubMed DOI PMC

Marschner P, Kandeler E, Marschner B. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem. 2003;35:453–61.

Mastný J, Bárta J, Kaštovská Eet al. . Decomposition of peatland DOC affected by root exudates is driven by specific r and K strategic bacterial taxa. Sci Rep. 2021;11:18677. 10.1038/s41598-021-97698-2. PubMed DOI PMC

McCune B, Mefford MJ. PC-ORD. Multivariate analysis of ecological data, v. 7. Gleneden Beach, Oregon: MjM Software Design, 2018.

Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic and human pathogenic microorganisms. FEMS Microbiol Rev. 2013;37:634–63. PubMed

Mitsch WJ, Gosselink JG. Wetlands. 3rd edn. New York: John Wiley and Sons, 2000.

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 Microb. 1993;59:695–700. PubMed PMC

Nakasaki K, Nguyen KK, Ballesteros FCet al. . Characterizing the microbial community involved in anaerobic digestion of lipid-rich wastewater to produce methane gas. Anaerobe. 2020;61:102082. 10.1016/j.anaerobe.2019.102082. PubMed DOI

Neubauer SC, Givler K, Valentine Set al. . Seasonal patterns and plant-mediate controls of subsurface wetland biogeochemistry. Ecology. 2005;86:3334–44.

Neumann G, Bott S, Ohler MAet al. . Root exudation and root development of lettuce (Lactuca sativa L. cv Tizian) as affected by different soils. Front Microbiol. 2014;5:2. 10.3389/fmicb.2014.00002. PubMed DOI PMC

Nguyen LTT, Osanai Y, Anderson ICet al. . Flooding and prolonged drought have differential legacy impacts on soil nitrogen cycling, microbial communities and plant productivity. Plant Soil. 2018;431:371–87.

Oksanen J, Blanchet FG, Friendly Met al. . vegan: community ecology package. R package version 2.5-7. 2020.<URL https://CRAN.R-project/package=vegan>. (18 July 2022 last date accessed).

Picek T, Kaštovská E, Edwards Ket al. . Short term effects of experimental eutrophication on carbon and nitrogen cycling in two types of wet grassland. Comm Ecol. 2008;9:81–90.

Pinheiro J, Bates D, DebRoy Set al. . _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–127, 2016. <URL: http://CRAN.R-project.org/package=nlme>. (17 April 2018 date last accessed).

Podosokorskaya OA, Kadnikov VV, Gavrilov SNet al. . Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ Microbiol. 2013;15:1759–71. PubMed

Pugnaire FI, Morillo JA, Penuelas Jet al. . Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems. Sci Adv. 2019;5:eaaz1834. 10.1126/sciadv.aaz1834. PubMed DOI PMC

R Core Team 2020. R version 4.0.0: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. URL https://www.R-project.org/. (19 November 2021 last date accessed).

R Core Team . 2021. R version 4.0.5: A language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. URL https://www.R-project.org/.18 July 2022 last day accessed).

Raaijmakers JM, Paulitz TC, Steinberg Cet al. . The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. 2009;321:341–61.

Reese AT, Lulow K, David LAet al. . Plant community and soil conditions individually affect soil microbial community assembly in experimental mesocosms. Ecol Evol. 2018;8:1196–205. PubMed PMC

Saggar S, Hedley C, Mackay AD. Partitioning and translocation of photosynthetically fixed 14C in grazed hill pastures. Biol Fert Soils. 1997;25:152–8.

Schellenberger S, Kolb S, Drake HL. Metabolic responses of novel cellulytic and saccharolytic agricultural soil Bacteria to oxygen. Environ Microbiol. 2010;12:845–61. PubMed

Schreiter S, Ding GC, Hauer Het al. . Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol. 2014;5:144. 10.3389/fmicb.2014.00144. PubMed DOI PMC

Sierra CA, Trumbore SE, Davidson EAet al. . Sensitivity of decomposition rates of soil organic matter with respect to simultaneous changes in temperature and moisture. J Adv Model Earth Syst. 2015;7:335–56.

Smith-Ramesh LM, Reynolds HL. the next frontier of plant-soil feedback research: unraveling context dependence across biotic and abiotic gradients. J Veg Sci. 2017;28:484–94.

Strickland MS, Rousk J. Considering fungal: bacterial dominance in soils—methods, controls and ecosystem implications. Soil Biol Biochem. 2010;42:1385–95.

Sutton-Grier AE, Megonigal JP. Plant species traits regulate methane production in freshwater wetland soils. Soil Biol Biochem. 2011;43:413–20.

Tahovská K, Choma M, Kaštovská Eet al. . Positive response of soil microbes to long-term nitrogen input in spruce forest: results from Gårdsj€on whole-catchment N-addition experiment. Soil Biol Biochem. 2020;143:107732. 10.1016/j.soilbio.2020.107732. DOI

Takai K, Moser DP, DeFlaun Met al. . Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol. 2001;67:5750–60. PubMed PMC

Tallowin JRB, Jefferson RG. Hay production from lowland seminatural grasslands: a review of implications for ruminant livestock systems. Grass Forage Sci. 1999;54:99–115.

Thompson LR, Sanders JG, McDonald Det al. . A communal catalogue reveals Earth's multiscale microbial diversity. Nature. 2017;551:457–63. PubMed PMC

Tian C, Wang C, Tian Yet al. . Root radial oxygen loss and the effects on rhizosphere microarea of two submerged plants. Pol J Environ Stud. 2015;24:1795–802.

Ueki A, Akasaka H, Suzuki Det al. . Xylanibacter oryzae gen. nov., sp. nov., a novel strictly anaerobic, Gram-negative, xylanolytic bacterium isolated from rice-plant residue in flooded rice-field soil in Japan. Int J System Evolut Microbiol. 2006;56:2215–21. PubMed

Unger IM, Motavalli PP, Muzika RM. Changes in soil chemical properties with flooding: a field laboratory approach. Agric Ecosyst Environ. 2009;131:105–10.

Visser EJW, Colmer TD, Blom CWPMet al. . Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ. 2000;23:1237–45.

Wang C, Liu D, Bai E. Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol Biochem. 2018;120:126–33.

Wang J, Wang D, Wang B. Soil bacterial diversity and its determinants in the riparian zone of the Lijiang River, China. Curr Sci. 2019;117:1324–32.

Wang X, Sharp CE, Jones GMet al. . Stable-isotope probing identifies uncultured Planctomycetes as primary degraders of a complex heteropolysaccharide in soil. Appl Environ Microbiol. 2015;81:4607–15. PubMed PMC

Watanabe T, Asakawa S, Hayano K. Long-term submergence of non-methanogenic oxic upland field soils helps to develop the methanogenic archaeal community as revealed by pot and field experiments. Pedosphere. 2020;30:62–72.

Weiss JV, Emerson D, Megonigal JP. Rhizosphere iron (III) deposition and reduction in a Juncus effusus L.-dominated wetland. Soil Sci Soc Am J. 2005;69:1861–70.

Wieczorek AS, Schmidt O, Chatzinotas Aet al. . Ecological functions of agricultural soil bacteria and microeukaryotes in chitin degradation: a case study. Front Microbiol. 2019;10:1293. 10.3389/fmicb.2019.01293. PubMed DOI PMC

Yarwood SA. The role of wetland microorganisms in plant-litter decomposition and soil organic matter formation: a critical review. FEMS Microbiol Ecol. 2018;94:fiy175. 10.1093/femsec/fiy175. PubMed DOI

Zhang Y, Shen H, He Xet al. . Fertilization shapes bacterial community structure by alteration of soil pH. Front Microbiol. 2017;8:1325. 10.3389/fmicb.2017.01325. PubMed DOI PMC

Zhao Z, Ge T, Gunina Aet al. . Carbon and nitrogen availability in paddy soil affects rice photosynthate allocation, microbial community composition, and priming: combining continuous 13C labeling with PLFA analysis. Plant Soil. 2019;445:137–52.

Zuur AF, Ieno EN, Walker NJet al. . Mixed Effects Models and Extensions in Ecology with R. New York: Springer, 2009.

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