Abstract
Soil fungi fill pivotal ecological roles in biogeochemical processes, particularly dominating decomposition of lignin. Little is known, however, about the responses of different fungal groups to climate warming with respect to bacteria. In this study, using barcode pyrosequencing, we showed that short-term (15 months) of field exposure of an alpine meadow to warming (elevated 1 and 2 °C) did not markedly alter the overall soil fungal community structures and α-diversity on Tibetan Plateau, but the average β-diversity dramatically decreased in response to warming. However, soil respiration rates were stimulated in the growing season, which significantly (P < 0.001) correlated with soil temperature. Particularly, warming triggered dramatic shifts in the community structure of dominate Ascomycota and rare taxa (relative abundance < 0.1 %). In addition, the abundances of specific Basidiomycota-affiliated members significantly increased, while Ascomycota showed a range of responses to warming. Collectively, we conclude that the fungal communities are resistant to short-term warming, though variations are observed in certain species and rare taxa. This report indicates that changes in a relatively small subset of the soil fungal community are sufficient to produce substantial changes in function, such as CO2 efflux rates.
Similar content being viewed by others
References
Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14:2898–2909
Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519
Allison SD, McGuir KL, Treseder KK (2010) Resistance of microbial and soil properties to warming treatment seven years after boreal fire. Soil Biol Biochem 42:1872–1878
Beare MH, Parmelee RW, Hendrix PF, Cheng W, Coleman DC, Crossley DA (1992) Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecol Monogr 62:569–591
Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456
Brazelton WJ, Ludwig KA, Sogin ML, Andreishcheva EN, Kelley DS, Shen C, Edwards LR, Baross JA (2010) Archaea and bacteria with surprising microdiversity show shifts in dominance over 1000-year time scales in hydrothermal chimneys. Proc Natl Acad Sci U S A 107:1612–1617
Bronson DR, Gower ST, Tanner M, Linder S, Van Herk I (2008) Responses of soil surface CO2 flux in a boreal forest to ecosystem warming. Glob Chang Biol 14:856–867
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al (2010) QIIME allows integration and analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267
Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc Biol Sci 366:2351–2363
Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD et al (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087
Crowther TW, Boddy L, Jones TH (2012) Functional and ecological consequences of saprotrophic fungus–grazer interactions. ISME J 6:1992–2001
Deacona LJ, Pryce-Millera EJ, Franklandb JC, Bainbridgea BW, Moorea PD, Robinson CH (2006) Diversity and function of decomposer fungi from a grassland soil. Soil Biol Biochem 38:7–20
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072
Deslippe JR, Hartmann M, Mohn WW, Simard SW (2011) Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Glob Chang Biol 17:1625–1636
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Flury S, Gessner MO (2011) Experimentally simulated global warming and nitrogen enrichment effects on microbial litter decomposers in a marsh. Appl Environ Microbiol 77:803–809
Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JG, Maire V et al (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96
Hawksworth DL (2004) Fungal diversity and its implications for genetic resource collections. Stud Mycol 50:9–17
Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystem 11:1157–1167
Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci U S A 107:5881–5886
Klein JA, Harte J, Zhao X (2004) Experimental warming causes large and rapid species loss, dampened by simulated grazing, on the Tibetan Plateau. Ecol Lett 7:1170–1179
Klein JA, Harte J, Zhao X (2007) Experimental warming, not grazing, decrease rangeland quality on the Tibetan Plateau. Ecol Appl 17:541–557
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Microbiol Rev 9:119–130
Liu X, Chen B (2000) Climatic warming in the Tibetan Plateau during recent decades. Int J Climatol 20:1729–1742
Lozupone CA, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Lu Z, Wu Q, Yu S, Zhang L (2006) Heat and water difference of active layers beneath different surface conditions near Beiluhe in Qinghai-Xizang Plateau. J Glaciol Geogryol 28:642–647
Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63
McGuire K, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91:2324–2332
Na L, Wang G, Yang Y, Gao Y, Liu G (2011) Plant production, carbon and nitrogen source pools, are strongly intensified by experimental warming in alpine ecosystems in the Qinghai-Tibet Plateau. Soil Biol Biochem 43:942–953
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810
Rinnan R, Michelsen A, Bååth E, Jonasson S (2007) Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob Chang Biol 13:28–39
Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B et al (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci U S A 103:12115–12120
Treseder KK, Holden SR (2013) Fungal carbon sequestration. Science 339:1528–1529
Treseder KK, Bent E, Borneman J, McGuire KL (2013) Shifts in fungal communities during decomposition of boreal forest litter. Fungal Ecol. doi:10.1016/j.funeco.2013.02.002
Tuomisto H (2010) A diversity of beta diversities: straightening up a concept gone awry. Part I. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33:2–22
Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936
Wagg C, Jansa J, Schmid B, van der Heijden MA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009
Xiong J, Liu Y, Lin X, Zhang H, Zeng J et al (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466
Yergeau E, Bokhorst S, Kang S, Zhou J, Greer CW, Aerts R, Kowalchuk GA (2011) Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME J 6:692–702
Yuste JC, Penuelas J, Estiarte M, Gracua-Mas J, Mattana S, Ogaya R et al (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Chang Biol 17:1475–1486
Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Chang Biol 11:266–277
Zhou J, Xue K, Xie J, Deng Y, Wu L, Cheng X et al (2012) Microbial mediation of carbon-cycle feedbacks to climate warming. Nat Clim Chang 2:106–110
Acknowledgments
We thank Maureen L. Coleman from University of Chicago for valuable comments on this manuscript. This work was supported by the National Natural Science Foundation of China to J. Xiong (41101228) and H. Chu (41071167), the ‘Hundred Talents Program’ of the Chinese Academy of Sciences to X. Xue and H. Chu, and the KC Wong Magna Fund in Ningbo University.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 1536 kb)
Rights and permissions
About this article
Cite this article
Xiong, J., Peng, F., Sun, H. et al. Divergent Responses of Soil Fungi Functional Groups to Short-term Warming. Microb Ecol 68, 708–715 (2014). https://doi.org/10.1007/s00248-014-0385-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-014-0385-6