in

Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt

  • 1.

    Bardgett RD, Van Der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505–11.

    CAS  PubMed  Article  Google Scholar 

  • 2.

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

    CAS  PubMed  Article  Google Scholar 

  • 3.

    De Vries FT, Shade A. Controls on soil microbial community stability under climate change. Front Microbiol. 2013;4:1–16.

    Article  Google Scholar 

  • 4.

    Allison SD, Martiny JBH. Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci. 2008;105:11512–9.

    CAS  PubMed  Article  Google Scholar 

  • 5.

    Leifeld J, Zimmermann M, Fuhrer J, Conen F. Storage and turnover of carbon in grassland soils along an elevation gradient in the Swiss Alps. Glob Chang Biol. 2009;15:668–79.

    Article  Google Scholar 

  • 6.

    Schirpke U, Leitinger G, Tasser E, Schermer M, Steinbacher M, Tappeiner U. Multiple ecosystem services of a changing Alpine landscape: past, present and future. Int J Biodivers Sci Ecosyst Serv Manag. 2013;9:123–35.

    PubMed  Article  Google Scholar 

  • 7.

    Beniston M. Is snow in the Alps receding or disappearing? Wiley Interdiscip Rev Clim Chang. 2012;3:349–58.

    Article  Google Scholar 

  • 8.

    Beniston M, Keller F, Koffi B, Goyette S. Estimates of snow accumulation and volume in the Swiss Alps under changing climatic conditions. Theor Appl Climatol. 2003;76:125–40.

    Article  Google Scholar 

  • 9.

    Monson RK, Burns SP, Williams MW, Delany AC, Weintraub M, Lipson DA. The contribution of beneath-snow soil respiration to total ecosystem respiration in a high-elevation, subalpine forest. Glob Biogeochem Cycles. 2006;20:1–13.

    Article  CAS  Google Scholar 

  • 10.

    Zhang Y, Wang S, Barr AG, Black TA. Impact of snow cover on soil temperature and its simulation in a boreal aspen forest. Cold Reg Sci Technol. 2008;52:355–70.

    Article  Google Scholar 

  • 11.

    Campbell JL, Ollinger SV, Flerchinger GN, Wicklein H, Hayhoe K, Bailey AS. Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA. Hydrol Process. 2010;24:2465–80.

    Google Scholar 

  • 12.

    Pederson GT, Gray ST, Woodhouse CA, Betancourt JL, Fagre DB, Littell JS, et al. The unusual nature of recent snowpack declines in the North American Cordillera. Science. 2011;333:332–5.

    CAS  PubMed  Article  Google Scholar 

  • 13.

    Gavazov K, Ingrisch J, Hasibeder R, Mills RTE, Buttler A, Gleixner G, et al. Winter ecology of a subalpine grassland: effects of snow removal on soil respiration, microbial structure and function. Sci Total Environ. 2017;590–591:316–324.

    PubMed  Article  CAS  Google Scholar 

  • 14.

    Buckeridge KM, Banerjee S, Siciliano SD, Grogan P. The seasonal pattern of soil microbial community structure in mesic low arctic tundra. Soil Biol Biochem. 2013;65:338–47.

    CAS  Article  Google Scholar 

  • 15.

    Puissant J, Cécillon L, Mills RTE, Robroek BJM, Gavazov K, De Danieli S, et al. Seasonal influence of climate manipulation on microbial community structure and function in mountain soils. Soil Biol Biochem. 2015;80:296–305.

    CAS  Article  Google Scholar 

  • 16.

    Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK. A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol. 2005;20:634–41.

    PubMed  Article  Google Scholar 

  • 17.

    Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, et al. Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology. 2007;88:1379–85.

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Schadt CW, Martin AP, Lipson DA, Schmidt SK. Seasonal dynamics of previously unknown fungal lineages in Tundra soils. Science. 2003;301:1359–61.

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Jefferies RL, Walker NA, Edwards KA, Dainty J. Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils? Soil Biol Biochem. 2010;42:129–35.

    CAS  Article  Google Scholar 

  • 20.

    Buckeridge KM, Grogan P. Deepened snow increases late thaw biogeochemical pulses in mesic low arctic tundra. Biogeochemistry. 2010;101:105–21.

    Article  Google Scholar 

  • 21.

    Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;88:1386–94.

    PubMed  Article  Google Scholar 

  • 22.

    Buckeridge KM, Grogan P. Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl Soil Ecol. 2008;39:210–22.

    Article  Google Scholar 

  • 23.

    Väisänen M, Gavazov K, Krab EJ, Dorrepaal E. The legacy effects of winter climate on microbial functioning after snowmelt in a subarctic Tundra. Micro Ecol. 2019;77:186–90.

    Article  Google Scholar 

  • 24.

    Darrouzet-Nardi A, Steltzer H, Sullivan PF, Segal A, Koltz AM, Livensperger C, et al. Limited effects of early snowmelt on plants, decomposers, and soil nutrients in Arctic Tundra soils. Ecol Evol. 2019;9:1820–44.

    PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Ernakovich JG, Hopping KA, Berdanier AB, Simpson RT, Kachergis EJ, Steltzer H, et al. Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change. Glob Chang Biol. 2014;20:3256–69.

    PubMed  Article  Google Scholar 

  • 26.

    Li W, Wu J, Bai E, Jin C, Wang A, Yuan F, et al. Response of terrestrial carbon dynamics to snow cover change: a meta-analysis of experimental manipulation (II). Soil Biol Biochem. 2016;103:388–93.

    CAS  Article  Google Scholar 

  • 27.

    Neuwinger I Bodenökologische. Untersuchungen im Gebiet Obergurgler Zirbenwald—Hohe Mut. In: Patzelt G (Hrsg.. (ed). MaB-Projekt Obergurgl. 1987. Universitätsverlag Wagner, Innsbruck, Austria, pp 173-90.

  • 28.

    Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911–917.

    CAS  Article  Google Scholar 

  • 29.

    Bardgett RD, Hobbs PJ, Frostegard A. Changes in soil fungal:bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biol Fertil Soils. 1996;22:261–4.

    Article  Google Scholar 

  • 30.

    Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE. 2008;3:e2836.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 31.

    Arenz BE, Schlatter DC, Bradeen JM, Kinkel LL. Blocking primers reduce co-amplification of plant DNA when studying bacterial endophyte communities. J Microbiol Methods. 2015;117:1–3.

    CAS  PubMed  Article  Google Scholar 

  • 32.

    Ihrmark K, Bödeker 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.

    CAS  PubMed  Article  Google Scholar 

  • 33.

    White TJ, Bruns T, Lee S, Taylor J. PCR protocols. 1990. Academic Press.

  • 34.

    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 35.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    R Core Team. R: a language and environment for statistical computing. 2019. R Foundation for Statistical Computing.

  • 37.

    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 38.

    Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, et al. UNITE: A database providing web-based methods for the molecular identification of ectomycorrhizal fungi. N. Phytol. 2005;166:1063–8.

    Article  CAS  Google Scholar 

  • 39.

    McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Illumina. bcl2fastq and bcl2fastq2 Conversion software. 2020. https://support.illumina.com/sequencing/sequencing

  • 41.

    Sáenz JS, Marques TV, Barone RSC, Cyrino JEP, Kublik S, Nesme J, et al. Oral administration of antibiotics increased the potential mobility of bacterial resistance genes in the gut of the fish Piaractus mesopotamicus. Microbiome. 2019;7:1–14.

    Article  Google Scholar 

  • 42.

    Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes. 2016;9:1–7.

    Article  Google Scholar 

  • 43.

    Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE. 2011;6:e17288.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    Menzel P, Ng KL, Krogh A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. 2016;7:11257.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 45.

    Tu Q, Lin L, Cheng L, Deng Y, He Z. NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics. 2019;35:1040–8.

    CAS  PubMed  Article  Google Scholar 

  • 46.

    First Y, Job P. GNU parallel: the command-line power tool | USENIX. 3: 42–47.

  • 47.

    Jackson CR, Tyler HL, Millar JJ. Determination of microbial extracellular enzyme activity in waters, soils, and sediments using high throughput microplate assays. J Vis Exp. 2013;80:e50399.

    Google Scholar 

  • 48.

    De Long JR, Semchenko M, Pritchard WJ, Cordero I, Fry EL, Jackson BG, et al. Drought soil legacy overrides maternal effects on plant growth. Funct Ecol. 2019;33:1400–10.

    PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium article in biology and fertility of soils. Biol Fertil Soils. 1988;6:68–72.

    CAS  Article  Google Scholar 

  • 50.

    Jones DL, Willett VB. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem. 2006;38:991–9.

    CAS  Article  Google Scholar 

  • 51.

    Ross DJ. Influence of sieve mesh size on estimates of microbial carbon and nitrogen by fumigation-extraction procedures in soils under pasture. Soil Biol Biochem. 1992;24:343–50.

    Article  Google Scholar 

  • 52.

    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.

    PubMed  Article  CAS  Google Scholar 

  • 53.

    Moorhead DDL, Sinsabaugh RRL. A theoretical model of litter decay and microbial interaction. Ecol Monogr. 2006;76:151–74.

    Article  Google Scholar 

  • 54.

    Zhou Y, Pope PB, Li S, Wen B, Tan F, Cheng S, et al. Omics-based interpretation of synergism in a soil-derived cellulose-degrading microbial community. Sci Rep. 2014;4:1–6.

    Google Scholar 

  • 55.

    Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev. 2002;66:506–77.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Bhatnagar JM, Peay KG, Treseder KK. Litter chemistry influences decomposition through activity of specific microbial functional guilds. Ecol Monogr. 2018;88:429–44.

    Article  Google Scholar 

  • 57.

    Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, et al. Stoichiometry of soil enzyme activity at global scale. Ecol Lett. 2008;11:1252–64.

    PubMed  Article  Google Scholar 

  • 58.

    Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 2012;6:1007–17.

    CAS  PubMed  Article  Google Scholar 

  • 59.

    Broadbent AAD, Orwin KH, Peltzer DA, Dickie IA, Mason NWH, Ostle NJ, et al. Invasive N-fixer impacts on litter decomposition driven by changes to soil properties not litter quality. Ecosystems. 2017;20:1–13.

    Article  CAS  Google Scholar 

  • 60.

    Prosser JI, Nicol GW. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 2012;20:523–31.

    CAS  PubMed  Article  Google Scholar 

  • 61.

    Verhamme DT, Prosser JI, Nicol GW. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011;5:1067–71.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 62.

    Brooks PD, Williams MW, Schmidt SK. Inorganic nitrogen and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry. 1998;43:1–15.

    Article  Google Scholar 

  • 63.

    Jaeger CH, Monson RK, Fisk MC, Schmidt SK. Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology. 1999;80:1883–91.

    Article  Google Scholar 

  • 64.

    Ashton IW, Miller AE, Bowman WD, Suding KN. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology. 2010;91:3252–60.

    PubMed  Article  Google Scholar 

  • 65.

    Bilbrough CJ, Welker JM, Bowman WD. Early spring nitrogen uptake by snow-covered plants: a comparison of Arctic and alpine plant function under the snowpack. Arct, Antarct Alp Res. 2000;32:404–11.

    Article  Google Scholar 

  • 66.

    Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D. Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia. 1996;105:53–63.

    PubMed  Article  Google Scholar 

  • 67.

    Wookey PA, Aerts R, Bardgett RD, Baptist F, Bråthen K, Cornelissen JHC, et al. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob Chang Biol. 2009;15:1153–72.

    Article  Google Scholar 


  • Source: Ecology - nature.com

    Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions

    Keeping an eye on the fusion future