Historical forest disturbance mediates soil microbial community responses to drought.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
revised:
11
06
2021
received:
24
03
2021
accepted:
02
08
2021
pubmed:
5
8
2021
medline:
18
3
2022
entrez:
4
8
2021
Statut:
ppublish
Résumé
Despite the abundance of studies demonstrating the effects of drought on soil microbial communities, the role of land use legacies in mediating these drought effects is unclear. To assess historical land use influences on microbial drought responses, we conducted a drought-rewetting experiment in soils from two adjacent and currently forested watersheds with distinct land use histories: an undisturbed 'reference' site and a 'disturbed' site that was clear-cut and converted to agriculture ~60 years prior. We incubated intact soil cores at either constant moisture or under a drought-rewet treatment and characterized bacterial and fungal communities using amplicon sequencing throughout the experiment. Bacterial alpha diversity decreased following drought-rewetting while fungal diversity increased. Bacterial beta diversity also changed markedly following drought-rewetting, especially in historically disturbed soils, while fungal beta diversity exhibited little response. Additionally, bacterial beta diversity in disturbed soils recovered less from drought-rewetting compared with reference soils. Disturbed soil communities also exhibited notable reductions in nitrifying taxa, increases in putative r-selected bacteria, and reductions in network connectivity following drought-rewetting. Overall, our study reveals historical land use to be important in mediating responses of soil bacterial communities to drought, which will influence the ecosystem-scale trajectories of these environments under ongoing and future climate change.
Identifiants
pubmed: 34347364
doi: 10.1111/1462-2920.15706
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
6405-6419Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Abarenkov, K., Nilsson, R.H., Larsson, K.-H., Alexander, I.J., Eberhardt, U., Erland, S., et al. (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186: 281-285.
Barnard, R.L., Osborne, C.A., and Firestone, M.K. (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7: 2229-2241.
Bastida, F., López-Mondéjar, R., Baldrian, P., Andrés-Abellán, M., Jehmlich, N., Torres, I.F., et al. (2019) When drought meets forest management: effects on the soil microbial community of a Holm oak forest ecosystem. Sci Total Environ 662: 276-286.
Bastida, F., Torres, I.F., Andrés-Abellán, M., Baldrian, P., López-Mondéjar, R., Větrovský, T., et al. (2017) Differential sensitivity of total and active soil microbial communities to drought and forest management. Glob Chang Biol 23: 4185-4203.
Bates, D., Maechler, M., Bolker, B. Walker, S., Christensen, R.H.B., et al. (2019) lme4: Linear Mixed-Effects Models using “Eigen” and S4.
Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57: 289-300.
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C., Al-Ghalith, G.A., et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37: 852-857.
Bouskill, N.J., Lim, H.C., Borglin, S., Salve, R., Wood, T.E., Silver, W.L., and Brodie, E.L. (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7: 384-394.
Burt, T.P., Ford Miniat, C., Laseter, S.H., and Swank, W.T. (2018) Changing patterns of daily precipitation totals at the Coweeta Hydrologic Laboratory, North Carolina, USA. Int J Climatol 38: 94-104.
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13: 581-583.
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., et al. (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108: 4516-4522.
Carini, P., Marsden, P.J., Leff, J.W., Morgan, E.E., Strickland, M.S., & Fierer, N. (2016). Relic DNA is abundant in soil and obscures estimates of soil microbial diversity.
Coyte, K.Z., Schluter, J., & Foster, K.R. (2015). The ecology of the microbiome: Networks, competition, and stability. Science 350: 663-666.
Csardi, G., and Nepusz, T. (2006) The igraph software package for complex network research. Int J Complex Syst 1695: 1-9.
De Vries, F.T., Griffiths, R.I., Bailey, M., Craig, H., Girlanda, M., Gweon, H.S., et al. (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9: 3033.
De Vries, F.T., Liiri, M.E., Bjørnlund, L., Bowker, M.A., Christensen, S., Setälä, H.M., and Bardgett, R.D. (2012) Land use alters the resistance and resilience of soil food webs to drought. Nat Clim Change London 2: 276-280.
Elliott, K.J., and Vose, J.M. (2011) The contribution of the Coweeta Hydrologic Laboratory to developing an understanding of long-term (1934-2008) changes in managed and unmanaged forests. For Ecol Manage 261: 900-910.
Ellis, E.C. (2011) Anthropogenic transformation of the terrestrial biosphere. Philos Trans R Soc A-Math Phys Eng Sci 369: 1010-1035.
Evans, S.E., and Wallenstein, M.D. (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109: 101-116.
Evans, S.E., and Wallenstein, M.D. (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17: 155-164.
Felsmann, K., Baudis, M., Gimbel, K., Kayler, Z.E., Ellerbrock, R., Bruehlheide, H., et al. (2015) Soil bacterial community structure responses to precipitation reduction and forest management in forest ecosystems across Germany. PLoS One 10: e0122539.
Fierer, N., Bradford, M.A., and Jackson, R.B. (2007) Toward an ecological classification of soil bacteria. Ecology 88: 1354-1364.
Fuchslueger, L., Bahn, M., Fritz, K., Hasibeder, R., & Richter, A. (2014). Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201: 916-927.
Gardes, M., and Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
Gragson, T.L., and Bolstad, P.V. (2006) Land use legacies and the future of southern Appalachia. Soc Nat Resour 19: 175-190.
Helvey, J., and Hewlett, J.D. (1962) The annual range of soil moisture under high rainfall in the southern Appalachians. J For 60: 485-486.
IPCC. (2013) . In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., et al. (eds). Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press.
Jangid, K., Williams, M.A., Franzluebbers, A.J., Schmidt, T.M., Coleman, D.C., and Whitman, W.B. (2011) Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem 43: 2184-2193.
Jansson, J.K., and Hofmockel, K.S. (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18: 35-46.
Keiser, A.D., Knoepp, J.D., and Bradford, M.A. (2016) Disturbance decouples biogeochemical cycles across forests of the southeastern US. Ecosystems 19: 50-61.
Kohout, P., Charvátová, M., Štursová, M., Mašínová, T., Tomšovský, M., and Baldrian, P. (2018) Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots. ISME J 12: 692-703.
Laseter, S.H., Ford, C.R., Vose, J.M., and Swift, L.W. (2012) Long-term temperature and precipitation trends at the Coweeta Hydrologic Laboratory, Otto, North Carolina, USA. Hydrol Res 43: 890-901.
Manzoni, S., Schimel, J.P., and Porporato, A. (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93: 930-938.
McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., et al. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6: 610-618.
Mushinski, R.M., Zhou, Y., Gentry, T.J., and Boutton, T.W. (2018) Bacterial metataxonomic profile and putative functional behavior associated with C and N cycle processes remain altered for decades after forest harvest. Soil Biol Biochem 119: 184-193.
Naylor, D., and Coleman-Derr, D. (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8: 2223.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., et al. (2019) vegan: Community Ecology Package.
Orwin, K.H., and Wardle, D.A. (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol Biochem 36: 1907-1912.
Osburn, E.D., and Barrett, J.E. (2020) Abundance and functional importance of complete ammonia-oxidizing bacteria (comammox) versus canonical nitrifiers in temperate forest soils. Soil Biol Biochem 145: 107801.
Osburn, E.D., McBride, S.G., Aylward, F.O., Badgley, B.D., Strahm, B.D., Knoepp, J.D., and Barrett, J.E. (2019) Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol 10: 2872.
Osburn, E.D., Simpson, J.S., Strahm, B.D., and Barrett, J.E. (2021) Land use history mediates soil biogeochemical responses to drought in temperate forest ecosystems. Ecosystems 24.
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., et al. (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12: 2825-2830.
Pimm, S.L. (1984) The complexity and stability of ecosystems. Nature 307: 321-326.
Placella, S.A., Brodie, E.L., and Firestone, M.K. (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci U S A 109: 10931-10936.
Preece, C., Verbruggen, E., Liu, L., Weedon, J.T., and Peñuelas, J. (2019) Effects of past and current drought on the composition and diversity of soil microbial communities. Soil Biol Biochem 131: 28-39.
R Core Development Team. (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Rillig, M.C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C.A., Buchert, S., Wulf, A., et al. (2019) The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366: 886-890.
Rodrigues, J.L.M., Pellizari, V.H., Mueller, R., Baek, K., Jesus, E.d.C., Paula, F.S., et al. (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci U S A 110: 988-993.
Schimel, J., Balser, T.C., and Wallenstein, M. (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88: 1386-1394.
Schimel, J., and Schaeffer, S.M. (2012) Microbial control over carbon cycling in soil. Front Microbiol 3: 348.
Schimel, J.P. (2018) Life in dry soils: effects of drought on soil microbial communities and processes. Annu Rev Ecol Evol Syst 49: 409-432.
Shade, A., Peter, H., Allison, S.D., Baho, D., Berga, M., Buergmann, H., et al. (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3: 417.
Shi, S., Nuccio, E.E., Shi, Z.J., He, Z., Zhou, J., and Firestone, M.K. (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19: 926-936.
Sun, Y., Chen, H.Y.H., Jin, L., Wang, C., Zhang, R., Ruan, H., and Yang, J. (2020) Drought stress induced increase of fungi:bacteria ratio in a poplar plantation. Catena 193: 104607.
White, T.J., Bruns, T., Lee, S., and Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for Phylogenetics. In PCR Protocols: Amsterdam, The Netherlands: Elsevier, pp. 315-322.
Williams, A.P., Cook, B.I., Smerdon, J.E., Bishop, D.A., Seager, R., and Mankin, J.S. (2017) The 2016 southeastern U.S. drought: an extreme departure from centennial wetting and cooling. J Geophys Res Atmos 122: 10888-10905.
Zhou, Z., Wang, C., and Luo, Y. (2018a) Effects of forest degradation on microbial communities and soil carbon cycling: a global meta-analysis. Glob Ecol Biogeogr 27: 110-124.
Zhou, Z., Wang, C., and Luo, Y. (2018b) Response of soil microbial communities to altered precipitation: a global synthesis. Glob Ecol Biogeogr 27: 1121-1136.