Fungal communities in European alpine soils are not affected by short-term in situ simulated warming than bacterial communities.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
received:
12
01
2022
accepted:
31
05
2022
pubmed:
13
6
2022
medline:
23
9
2022
entrez:
12
6
2022
Statut:
ppublish
Résumé
The impact of global warming on biological communities colonizing European alpine ecosystems was recently studied. Hexagonal open top chambers (OTCs) were used for simulating a short-term in situ warming (estimated around 1°C) in some alpine soils to predict the impact of ongoing climate change on resident microbial communities. Total microbial DNA was extracted from soils collected either inside or outside the OTCs over 3 years of study. Bacterial and fungal rRNA copies were quantified by qPCR. Metabarcoding sequencing of taxonomy target genes was performed (Illumina MiSeq) and processed by bioinformatic tools. Alpha- and beta-diversity were used to evaluate the structure of bacterial and fungal communities. qPCR suggests that, although fluctuations have been observed between soils collected either inside and outside the OTCs, the simulated warming induced a significant (p < 0.05) shift only for bacterial abundance. Likewise, significant (p < 0.05) changes in bacterial community structure were detected in soils collected inside the OTCs, with a clear increase of oligotrophic taxa. On the contrary, fungal diversity of soils collected either inside and outside the OTCs did not exhibit significant (p < 0.05) differences, suggesting that the temperature increase in OTCs compared to ambient conditions was not sufficient to change fungal communities.
Identifiants
pubmed: 35691701
doi: 10.1111/1462-2920.16090
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4178-4192Informations de copyright
© 2022 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Adamczyk, M., Hagedorn, F., Wipf, S., Donhauser, J., Vittoz, P., Rixen, C. et al. (2019) The soil microbiome of GLORIA Mountain summits in the Swiss Alps. Front Microbiol, 10, 1080.
Adamczyk, M., Rüthi, J. & Frey, B. (2021) Root exudates increase soil respiration and alter microbial community structure in alpine permafrost and active layer soils. Environ Microbiol, 23, 2152-2168.
Arraiano-Castilho, R., Bidartondo, M.I., Niskanen, T., Clarkson, J.J., Brunner, I., Zimmermann, S. et al. (2021) Habitat specialisation controls ectomycorrhizal fungi above the treeline in the European Alps. N Phytol, 229, 2901-2916.
Baldrian, P., Větrovský, T., Lepinay, C. & Kohout, P. (2021) High-throughput sequencing view on the magnitude of global fungal diversity. Fungal Divers, 19, 1-9.
Bell, T.H., Klironomos, J.N. & Henry, H.A.L. (2010) Season responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J, 74, 820-828.
Biasi, C., Meyer, H., Rusalimova, O., Hammerle, R., Kaiser, C. & Baranyi, C. (2008) Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil, 307, 191-205.
Blankinship, J.C., Niklaus, P.A. & Hungate, B.A. (2011) A meta-analysis of responses of soil biota to global change. Oecologia, 165, 553-565.
Buzzini, P., Turchetti, B. & Yurkov, A. (2018) Extremophilic yeasts: the toughest yeasts around? Yeast, 35, 487-497.
Buzzini, P., Turk, M., Perini, L., Turchetti, B. & Gunde-Cimerman, N. (2017) Yeasts in polar and subpolar habitats. In: Buzzini, P., Lachance, M.A. & Yurkov, A. (Eds.) Yeasts in Natural Ecosystems: Diversity. Berlin, Germany: Springer-Verlag, pp. 331-365.
Cannone, N., Diolaiuti, G., Guglielmin, M. & Smiraglia, C. (2008) Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps. Ecol Appl, 18, 637-648.
Cannone, N. & Pignatti, S. (2014) Ecological responses of plant species and communities to climate warming: upward shift or range filling processes? Clim Change, 123, 201-214.
Cannone, N., Sergio, S. & Guglielmin, M. (2007) Unexpected impacts of climate change on alpine vegetation. Front Ecol Environ, 5, 360-364.
Carrasco, M., Rozas, J.M., Barahona, S., Alcaıno, J., Cifuentes, V. & Baeza, M. (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol, 12, 251-259.
Cavicchioli, R., Ripple, W.J., Timmis, K.N., Azam, F., Bakken, L.R., Baylis, M. et al. (2019) Scientists' warming to humanity: microorganisms and climate change. Nat Rev Microbiol, 17, 569-586.
Collins, M., Knutti, R., Arblaster, J., Dufresne, J.L., Fichefet, T., Friedlingstein, P. et al. (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker, T.F., Qin, D., Plattner, G.K., Tignor, M., Allen, S.K., Boschung, J. et al. (Eds.) Climate Change, 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York, NY, USA: Cambridge University Press, pp. 1029-1036.
Compant, S., van der Heijden, M.G. & Sessitsch, A. (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol, 73, 197-214.
D'Alò, F., Baldrian, P., Odriozola, I., Morais, D., Větrovský, T., Zucconi, L. et al. (2022) Composition and functioning of the soil microbiome in the highest altitudes of the Italian Alps and potential effects of climate change. FEMS Microbiol Ecol, 98, fiac025.
D'Alò, F., Odriozola, I., Baldrian, P., Zucconi, L., Ripa, C., Cannone, N. et al. (2021) Microbial activity in alpine soils under climate change. Sci Total Environ, 783, 147012.
de Menezes, A.B., Richardson, A.E. & Thrall, P.H. (2017) Linking fungal-bacterial cooccurrences to soil ecosystem function. Curr Opin Microbiol, 37, 135-141.
Dedysh, S.N. & Ivanova, A.A. (2019) Planctomycetes in boreal and subarctic wetlands: diversity patterns and potential ecological functions. FEMS Microbiol Ecol, 95, fiy227.
Defrenne, C.E., Philpott, T.J., Guichon, S.H., Roach, W.J., Pickles, B.J. & Simard, S.W. (2019) Shifts in ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior Douglas-fir forests of western Canada. Front Plant Sci, 10, 643.
0.02w?>Donhauser, J. & Frey, B. (2018) Alpine soil microbial ecology in a changing world. FEMS Microbiol Ecol, 94, fiy099.
Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460-2461.
Egidi, E., Delgado-Baquerizo, M., Plett, J.M., Wang, J., Eldridge, D.J., Bardgett, R.D. et al. (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nat Commun, 10, 2369.
Erschbamer, B., Kiebacher, T., Mallaun, M. & Unterluggauer, P. (2009) Short-term signals of climate change along an altitudinal gradient in the South Alps. Plant Ecol, 202, 79-89.
Fierer, N., Jackson, J.A., Vilgalys, R. & Jackson, R.B. (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol, 71, 4117-4120.
Fierer, N., Schimel, J.P. & Holden, P.A. (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microbiol Ecol, 45, 63-71.
França, L., Sannino, C., Turchetti, B., Buzzini, P. & Margesin, R. (2016) Seasonal and altitudinal changes of culturable bacterial and yeast diversity in alpine forest soils. Extremophiles, 20, 855-873.
Franzetti, A., Pittino, F., Gandolfi, I., Azzoni, R.S., Diolaiuti, G., Smiraglia, C. et al. (2020) Early ecological succession patterns of bacterial, fungal and plant communities along a chronosequence in a recently deglaciated area of the Italian Alps. FEMS Microbiol Ecol, 96, fiaa165.
Frey, B., Rieder, S.R., Brunner, I., Plötze, M., Koetzsch, S., Lapanje, A. et al. (2010) Weathering-associated bacteria from the Damma glacier forefield: physiological capabilities and impact on granite dissolution. Appl Environ Microbiol, 76, 4788-4796.
Frey, B., Rime, T., Phillips, M., Stierli, B., Hajdas, I., Widmer, F. et al. (2016) Microbial diversity in European alpine permafrost and active layers. FEMS Microbiol Ecol, 92, 1-17.
Gray, S.B., Classen, A.T., Kardol, P., Yermakov, Z. & Mille, M.R. (2011) Multiple climate change factors interact to alter soil microbial community structure in an old-field ecosystem. Soil Sci Soc Am J, 75, 2217-2226.
Griffiths, B.S. & Philippot, L. (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev, 37, 112-129.
Gutknecht, J.L., Field, C.B. & Balser, T.C. (2012) Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Global Change Biol, 18, 2256-2269.
Hansen, G. & Stone, D. (2015) Assessing the observed impact of anthropogenic climate change. Nat Clim Change, 6, 532-537.
Heydari, S. & Pirzad, A. (2020) Mycorrhizal fungi and Thiobacillus co-inoculation improve the physiological indices of Lallemantia iberica under salinity stress. Curr Microbiol, 77, 2523-2534.
Ho, A., Di Lonardo, D.P. & Bodelier, P.L.E. (2017) Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiol Ecol, 93, fix006.
IPCC. (2018) An IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. In: Masson-Delmotte, V., Zhai, P., Pörtner, H.O., Roberts, D., Skea, J., Shukla, P.R. et al. (Eds.) Global Warming of 1.5°C. The Intergovernmental Panel on Climate Change, Geneva, Switzerland: IPCC.
Janssen, P.H. (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol, 72, 1719-1728.
Jumpponen, A. & Jones, K.L. (2014) Tallgrass prairie soil fungal communities are resilient to climate change. Fungal Ecol, 10, 44-57.
Klarenberg, I.J., Keuschnig, C., Russi Colmenares, A.J., Warshan, D., Jungblut, A.D., Jónsdóttir, I.S. et al. (2021) Long-term warming effects on the microbiome and nifH gene abundance of a common moss species in sub-Arctic tundra. New Phytol, 234, 2044-2056.
Klarenberg, I.J., Keuschnig, C., Warshan, D., Jónsdóttir, I.S. & Vilhelmsson, O. (2020) The total and active bacterial community of the chlorolichen Cetraria islandica and its response to long-term warming in sub-Arctic tundra. Front Microbiol, 11, 3299.
Klassen, R., Schaffrath, R., Buzzini, P. & Ganter, P.F. (2017) Antagonistic interactions and killer yeasts. In: Buzzini, P., Lachance, M.A. & Yurkov, A. (Eds.) Yeasts in Natural Ecosystems: Ecology. Heidelberg, Germany: Springer, pp. 229-275.
Koch, I.H., Gich, F., Dunfield, P.F. & Overmann, J. (2008) Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol, 58, 1114-1122.
Krishnan, A., Convey, P., Gonzalez-Rocha, G. & Alias, S.A. (2016) Production of extracellular hydrolase enzymes by fungi from King George Island. Polar Biol, 39, 65-76.
Legendre, P. & Legendre, L. (1998) Numerical Ecology. Amsterdam, The Netherlands: Elsevier Sciences.
Li, G., Kim, S., Park, M. & Son, Y. (2017) Short-term effects of experimental warming and precipitation manipulation on soil microbial biomass C and N, community substrate utilization patterns and community composition. Pedosphere, 27, 714-724.
Lindahl, B.D., Nilsson, R.H., Tedersoo, L., Abarenkov, K., Carlsen, T., Kjøller, R.I. et al. (2013) Fungal community analysis by high-throughput sequencing of amplified markers - A user's guide. New Phytol, 199, 288-299.
Ludwig, W., Bauer, S.H., Bauer, M., Held, I., Kirchhof, G., Schulze, R. et al. (1997) Detection and in situ identification of representatives of a widely distributed new bacterial phylum. FEMS Microbiol Lett, 153, 181-190.
Luláková, P., Perez-Mon, C., Šantrůčková, H., Ruethi, J. & Frey, B. (2019) High-alpine permafrost and active-layer soil microbiomes differ in their response to elevated temperatures. Front Microbiol, 10, 668.
Malfasi, F. & Cannone, N. (2020) Climate warming persistence triggered tree ingression after shrub encroachment in a high alpine tundra. Ecosystems, 23, 1657-1675.
Mania, I., D'Amico, M., Freppaz, M. & Gorra, R. (2016) Driving factors of soil microbial ecology in alpine, mid-latitude patterned grounds (NW Italian Alps). Biol Fertil Soils, 52, 1135-1148.
Margesin, R., Minerbi, S. & Schinner, F. (2014) Long-term monitoring of soil microbiological activities in two forest sites in South Tyrol in the Italian Alps. Microbes Environ, 29, 277-285.
Marion, G.M., Henry, G.H.R., Freckman, D.W., Johnstone, J., Jones, G., Jones, M.H. et al. (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Global Change Biol, 3, 20-32.
Marzorati, M., Wittebolle, L., Boon, N., Daffonchio, D. & Verstraete, W. (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol, 10, 1571-1581.
Mello, A., Napoli, C., Murat, C., Morin, E., Marceddu, G. & Bonfante, P. (2011) ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle grounds. Mycologia, 103, 1184-1193.
Mostafavin, S.R., Pirdashti, H., Ramaznpour, M.R., Andarkhoran, A.A. & Shahsavari, A. (2008) Effect of mycorrhizal, Thiobacillus and sulfur nutrition on the chemical composition of soybean (Glycine max L.) Merr seed. Pak J Biol Sci, 11, 826-835.
Nara, K. & Hogetsu, T. (2004) Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology, 85, 1700-1707.
Nesje, A. & Dahl, S.O. (2000) Glaciers and Environmental Changes. London: Arnold.
Nguyen, N.H., Song, Z., Bates, S.T., Branco, S., Tedersoo, L., Menke, J. et al. (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fung Ecol, 20, 241-248.
Onofri, S., de la Torre, R., de Vera, J.P., Ott, S., Zucconi, L., Selbmann, L. et al. (2012) Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology, 12, 508-516.
Palmer, J.M., Jusino, M.A., Banik, M.T. & Linder, D.L. (2018) Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data. Peer J, 6, e4925.
Parolo, G. & Rossi, G. (2008) Upward migration of vascular plants following a climate warming trend in the Alps. Basic Appl Ecol, 9, 100-107.
Pauli, H., Gottfried, M., Dullinger, S., Abdaladze, O., Akhalkatsi, M., Benito Alonso, J.L. et al. (2012) Recent plant diversity changes on Europe's mountain summits. Science, 336, 353-355.
Pearce, D.A., Newsham, K.K., Thorne, M.A., Calvo-Bado, L., Krsek, M., Laskaris, P. et al. (2012) Metagenomic analysis of a southern maritime Antarctic soil. Front Microbiol, 3, 403.
Pellissier, L., Niculita-Hirzel, H., Dubuis, A., Pagni, M., Guex, N., Ndiribe, C. et al. (2014) Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps. Mol Ecol, 23, 4274-4290.
Pellissier, L., Pinto-Figueroa, E., Niculita-Hirzel, H., Moora, M., Villard, L., Goudet, J. et al. (2013) Plant species distributions along environmental gradients: do belowground interactions with fungi matter? Front Plant Sci, 4, 500.
Perez-Mon, C., Stierli, B., Plötze, M. & Frey, B. (2022) Fast and persistent responses of alpine permafrost microbial communities to in situ warming. Sci Total Environ, 807, 150720.
Petroselli, C., Montalbani, E., La Porta, G., Crocchianti, S., Moroni, B., Casagrande, C. et al. (2021) Characterization of long-range transported bioaerosols in the Central Mediterranean. Sci Total Environ, 763, 143010.
Philippot, L., Griffiths, B.S. & Langenheder, S. (2021) Microbial community resilience across ecosystems and multiple disturbances. Microbiol Mol Biol Rev, 85, e00026-20.
Pittino, F., Maglio, M., Gandolfi, I., Azzoni, R., Diolaiuti, G., Ambrosini, R. et al. (2018) Bacterial communities of cryoconite holes of a temperate alpine glacier show both seasonal trends and year-to-year variability. Ann Glaciol, 59, 1-9.
Rime, T., Hartmann, M., Brunner, I., Widmer, F., Zeyer, J. & Frey, B. (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol Ecol, 24, 1091-1108.
Rime, T., Hartmann, M. & Frey, B. (2016) Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. ISME J, 10, 1625-1641.
Rinnan, R. & Bååth, E. (2009) Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Appl Environ Microbiol, 75, 3611-3620.
Rinnan, R., Michelsen, A., Baat, E. & Jonasson, S. (2007) Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Appl Soil Ecol, 39, 271-281.
Rodriguez, R.J., White, J.F., Jr., Arnold, A.E. & Redman, A.R.A. (2009) Fungal endophytes: diversity and functional roles. New Phytol, 182, 314-330.
Romero-Olivares, A.L., Allison, S.D. & Treseder, K.K. (2017) Soil microbes and their response to experimental warming over time: a meta-analysis of field studies. Soil Biol Biochem, 107, 32-40.
Samaniego, L., Thober, S., Kumar, R., Wanders, N., Rakovec, O., Pan, M. et al. (2018) Anthropogenic warming exacerbates European soil moisture droughts. Nat Clim Change, 8, 421-426.
Sandvik, S.M., Heegaard, E., Elven, R. & Vandvik, V. (2004) Responses of alpine snowbed vegetation to long-term experimental warming. Ecoscience, 11, 150-159.
Sannino, C., Borruso, L., Mezzasoma, A., Battistel, D., Ponti, S., Turchetti, B. et al. (2021) Abiotic factors affecting the bacterial and fungal diversity of permafrost in a rock glacier in the Stelvio Pass (Italian Central Alps). Appl Soil Ecol, 166, 104079.
Sannino, C., Borruso, L., Smiraglia, C., Bani, A., Mezzasoma, A., Brusetti, L. et al. (2020) Dynamics of in situ growth and taxonomic structure of fungal communities in alpine supraglacial debris. Fungal Ecol, 44, 100891.
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S. et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biol, 12, R60.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D. et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res, 13, 2498-2504.
Siles, J.A. & Margesin, R. (2016) Abundance and diversity of bacterial, archaeal and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microb Ecol, 72, 207-220.
Sorensen, J.W. & Shade, A. (2020) Dormancy dynamics and dispersal contribute to soil microbiome resilience. Philos Trans R Soc B, 375, 20190255.
Steinbauer, M.J., Grytnes, J.A., Jurasinski, G., Kulonen, A., Lenoir, J., Pauli, H. et al. (2018) Accelerated increase in plant species richness on mountain summits is linked to warming. Nature, 556, 231-234.
Su, Y., Jiang, X., Wu, W., Wang, M., Hamid, M.I., Xiang, M. et al. (2016) Genomic, transcriptomic, and proteomic analysis provide insights into the cold adaptation mechanism of the obligate psychrophilic fungus Mrakia psychrophila. G3-Genes Genom Genet, 6, 3603-3613.
Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N.S., Wijesundera, R. et al. (2014) Global diversity and geography of soil fungi. Science, 346, 1256688.
Ter Braak, C.J.F., and Šmilauer, P. (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination, ver. 4.5. Ithaca, NY, USA.
Turchetti, B., Goretti, M., Branda, E., Diolaiuti, G., D'Agata, C., Smiraglia, C. et al. (2013) Influence of abiotic variables on culturable yeast diversity in two distinct alpine glaciers. FEMS Microbiol Ecol, 86, 327-340.
Wang, X., Dong, S., Gao, Q., Zhou, H., Liu, S., Su, X. et al. (2014) Effects of short-term and long-term warming on soil nutrients, microbial biomass and enzyme activities in an alpine meadow on the Qinghai-Tibet Plateau of China. Soil Biol Biochem, 76, 140-142.
Whittaker, R.H. (1972) Evolution and measurement of species diversity. Taxon, 21, 213-251.
Wieser, G. (2020) Alpine and polar treelines in a changing environment. Forests, 11, 254.
Xiong, J., Peng, F., Sun, H., Xue, X. & Chu, H. (2014) Divergent responses of soil fungi functional groups to short-term warming. Microb Ecol, 68, 708-715.
Xue, K., Xie, J., Zhou, A., Liu, F., Li, D., Wu, L. et al. (2016) Warming alters expressions of microbial functional genes important to ecosystem functioning. Front Microbiol, 7, 668.
Yabe, S., Aiba, Y., Sakai, Y., Hazaka, M. & Yokota, A. (2011) Thermogemmatispora onikobensis gen. nov., sp. nov. and Thermogemmatispora foliorum sp. nov., isolated from fallen leaves on geothermal soils, and description of Thermogemmatisporaceae fam. nov. and Thermogemmatisporales ord. nov. within the class Ktedonobacteria. Int J Syst Evol Microbiol, 61, 903-910.
Yang, Y., Halbritter, A.H., Klanderud, K., Telford, R.J., Wang, G. & Vandvik, V. (2018) Transplants, open top chambers (OTCs) and gradient studies ask different questions in climate change effects studies. Front Plant Sci, 9, 1574.
Yao, F., Yang, S., Wang, Z., Wang, X., Ye, J., Wang, X. et al. (2017) Microbial taxa distribution is associated with ecological trophic cascades along an elevation gradient. Front Microbiol, 8, 2071.
Yashiro, E., Pinto-Figueroa, E., Buri, A., Spangenberg, J.E., Adatte, T., Niculita-Hirzel, H. et al. (2016) Local environmental factors drive divergent grassland soil bacterial communities in the western Swiss Alps. Appl Environ Microbiol, 82, 6303-6316.
Yuan, M.M., Guo, X., Wu, L., Zhang, Y., Xiao, N., Ning, D. et al. (2021) Climate warming enhances microbial network complexity and stability. Nat Clim Change, 11, 343-348.
Zemp, M., Haeberli, W., Hoelzle, M. & Paul, F. (2006) Alpine glaciers to disappear within decades? Geophys Res Lett, 33, L13504.
Zhang, H. & Fu, G. (2021) Responses of plant, soil bacterial and fungal communities to grazing vary with pasture seasons and grassland types, Northern Tibet. Land Degrad Dev, 32, 1821-1832.
Zhang, K., Shi, Y.U., Jing, X., He, J.S., Sun, R., Yang, Y. et al. (2016) Effects of short-term warming and altered precipitation on soil microbial communities in alpine grassland of the Tibetan Plateau. Front Microbiol, 7, 1032.
Zhang, X., Shen, Z. & Fu, G. (2015) A meta-analysis of the effects of experimental warming on soil carbon and nitrogen dynamics on the Tibetan plateau. Appl Soil Ecol, 87, 32-38.
Zheng, H., Liu, Y., Chen, Y., Zhang, J., Li, H., Wang, L. et al. (2020) Short-term warming shifts microbial nutrient limitation without changing the bacterial community structure in an alpine timberline of the eastern Tibetan plateau. Geoderma, 360, 113985.
Zheng, Y., Wang, C.M., Sakai, Y., Abe, K., Yokota, A. & Yabe, S. (2019) Thermogemmatispora aurantia sp. nov. and Thermogemmatispora argillosa sp. nov., within the class Ktedonobacteria, and emended description of the genus Thermogemmatispora. Int J Syst Evol Microbiol, 69, 1744-1750.
Zong, N., and Fu, G. (2021) Variations in species and function diversity of soil fungal community along a desertification gradient in an alpine steppe. Ecological Indicators 2021 v.131, p. 108197.