Continental-scale niche differentiation of dominant topsoil archaea in drylands.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
11 2022
Historique:
received: 30 03 2021
accepted: 07 06 2022
pubmed: 17 6 2022
medline: 19 11 2022
entrez: 16 6 2022
Statut: ppublish

Résumé

Archaea represent a diverse group of microorganisms often associated with extreme environments. However, an integrated understanding of biogeographical patterns of the specialist Haloarchaea and the potential generalist ammonia-oxidizing archaea (AOA) across large-scale environmental gradients remains limited. We hypothesize that niche differentiation determines their distinct distributions along environmental gradients. To test the hypothesis, we use a continental-scale research network including 173 dryland sites across northern China. Our results demonstrate that Haloarchaea and AOA dominate topsoil archaeal communities. As hypothesized, Haloarchaea and AOA show strong niche differentiation associated with two ecosystem types mainly found in China's drylands (i.e. deserts vs. grasslands), and they differ in the degree of habitat specialization. The relative abundance and richness of Haloarchaea are higher in deserts due to specialization to relatively high soil salinity and extreme climates, while those of AOA are greater in grassland soils. Our results further indicate a divergence in ecological processes underlying the segregated distributions of Haloarchaea and AOA. Haloarchaea are governed primarily by environmental-based processes while the more generalist AOA are assembled mostly via spatial-based processes. Our findings add to existing knowledge of large-scale biogeography of topsoil archaea, advancing our predictive understanding on changes in topsoil archaeal communities in a drier world.

Identifiants

pubmed: 35706137
doi: 10.1111/1462-2920.16099
doi:

Substances chimiques

Ammonia 7664-41-7
Soil 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5483-5497

Informations de copyright

© 2022 Society for Applied Microbiology and John Wiley & Sons Ltd.

Références

Adair, K.L. & Schwartz, E. (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona USA. Microbial Ecology, 56, 420-426.
Auguet, J.C., Barberán, A. & Casamayor, E.O. (2010) Global ecological patterns in uncultured Archaea. The ISME Journal, 4, 182-190.
Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M. et al. (2018) Structure and function of the global topsoil microbiome. Nature, 560, 233-237.
Baker, B.J., De Anda, V., Seitz, K.W., Dombrowski, N., Santoro, A.E. & Lloyd, K.G. (2020) Diversity, ecology and evolution of Archaea. Nature Microbiology, 5, 887-900.
Banerjee, S., Schlaeppi, K. & van der Heijden, M.G.A. (2018) Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology, 16, 567-576.
Barberán, A., Bates, S.T., Casamayor, E.O. & Fierer, N. (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. The ISME Journal, 6, 343-351.
Bates, S.T., Berg-Lyons, D., Caporaso, J.G., Walters, W.A., Knight, R. & Fierer, N. (2011) Examining the global distribution of dominant archaeal populations in soil. The ISME Journal, 5, 908-917.
Berdugo, M., Maestre, F.T., Kéfi, S., Gross, N., Le Bagousse-Pinguet, Y. & Soliveres, S. (2019) Aridity preferences alter the relative importance of abiotic and biotic drivers on plant species abundance in global drylands. Journal of Ecology, 107, 190-202.
Berdugo, M., Delgado-Baquerizo, M., Soliveres, S., Hernández-Clemente, R., Zhao, Y.C., Gaitán, J.J. et al. (2020) Global ecosystem thresholds driven by aridity. Science, 367, 787-790.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K. et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336.
Chaban, B., Ng, S.Y. & Jarrell, K.F. (2006) Archaeal habitats - from the extreme to the ordinary. Canadian Journal of Microbiology, 52, 73-116.
Chen, X.P., Zhu, Y.G., Xia, Y., Shen, J.P. & He, J.Z. (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environmental Microbiology, 10, 1978-1987.
Chinese Academy of Sciences. (2001) Vegetation atlas of China. Beijing, China: Science Press.
Chu, H.Y., Neufeld, J.D., Walker, V.K. & Grogan, P. (2011) The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a low Arctic tundra landscape. Soil Science Society of America Journal, 75, 1756-1765.
Delgado-Baquerizo, M., Gallardo, A., Wallenstein, M.D. & Maestre, F.T. (2013a) Vascular plants mediate the effects of aridity and soil properties on ammonia-oxidizing bacteria and archaea. FEMS Microbiology Ecology, 85, 273-282.
Delgado-Baquerizo, M., Maestre, F.T., Gallardo, A., Bowker, M.A., Wallenstein, M.D., Quero, J.L. et al. (2013b) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature, 502, 672-676.
Delgado-Baquerizo, M., Maestre, F.T., Gallardo, A., Eldridge, D.J., Soliveres, S., Bowker, M.A. et al. (2016a) Human impacts and aridity differentially alter soil N availability in drylands worldwide. Global Ecology and Biogeography, 25, 36-45.
Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitán, J.J., Encinar, D. et al. (2016b) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications, 7, 10541.
Delgado-Baquerizo, M., Bissett, A., Eldridge, D.J., Maestre, F.T., He, J.-Z., Wang, J.-T. et al. (2017) Palaeoclimate explains a unique proportion of the global variation in soil bacterial communities. Nature Ecology & Evolution, 1, 1339-1347.
Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-González, A., Eldridge, D.J., Bardgett, R.D. et al. (2018) A global atlas of the dominant bacteria found in soil. Science, 359, 320-325.
Devictor, V., Julliard, R. & Jiguet, F. (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos, 117, 507-514.
Dolédec, S., Chessel, D. & Gimaret-Carpentier, C. (2000) Niche separation in community analysis: a new method. Ecology, 81, 2914-2927.
Egidi, E., Delgado-Baquerizo, M., Plett, J.M., Wang, J.T., Eldridge, D.J., Bardgett, R.D. et al. (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nature Communications, 10, 2369.
Erguder, T.H., Boon, N., Wittebolle, L., Marzorati, M. & Verstraete, W. (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology Reviews, 33, 855-869.
Fick, S.E. & Hijmans, R.J. (2017) Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302-4315.
Fierer, N. & Jackson, R.B. (2006) The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America, 103, 626-631.
Fournier, B., Vázquez-Rivera, H., Clappe, S., Donelle, L., Braga, P.H.P. & Peres-Neto, P.R. (2020) The spatial frequency of climatic conditions affects niche composition and functional diversity of species assemblages: the case of angiosperms. Ecology Letters, 23, 254-264.
Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E. & Oakley, B.B. (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America, 102, 14683-14688.
Genderjahn, S., Alawi, M., Mangelsdorf, K., Horn, F. & Wagner, D. (2018) Desiccation- and saline-tolerant bacteria and archaea in Kalahari pan sediments. Frontiers in Microbiology, 9, 2082.
Grayston, S.J., Wang, S., Campbell, C.D. & Edwards, A.C. (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biology and Biochemistry, 30, 369-378.
Griffiths, R.I., Thomson, B.C., James, P., Bell, T., Bailey, M. & Whiteley, A.S. (2011) The bacterial biogeography of British soils. Environmental Microbiology, 13, 1642-1654.
Hanson, C.A., Fuhrman, J.A., Horner-Devine, M.C. & Martiny, J.B.H. (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nature Reviews Microbiology, 10, 497-506.
Hu, W.G., Ran, J.Z., Dong, L.W., Du, Q.J., Ji, M.F., Yao, S.R. et al. (2021) Aridity-driven shift in biodiversity-soil multifunctionality relationships. Nature Communications, 12, 5350.
Jiang, H.C., Dong, H.L., Yu, B.S., Liu, X.Q., Li, Y.L., Ji, S.S. et al. (2007) Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environmental Microbiology, 9, 2603-2621.
Jiao, S., Xu, Y.Q., Zhang, J. & Lu, Y.H. (2019) Environmental filtering drives distinct continental atlases of soil archaea between dryland and wetland agricultural ecosystems. Microbiome, 7, 15.
Ke, X.B., Angel, R., Lu, Y.H. & Conrad, R. (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environmental Microbiology, 15, 2275-2292.
Ke, X.B., Lu, Y.H. & Conrad, R. (2014) Different behaviour of methanogenic archaea and Thaumarchaeota in rice field microcosms. FEMS Microbiology Ecology, 87, 18-29.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-1874.
Langenheder, S. & Székely, A.J. (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. The ISME Journal, 5, 1086-1094.
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W. et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442, 806-809.
Levins, R. (1968) Evolution in changing environments: some theoretical explorations. Princeton, USA: Princeton University Press.
Liao, J.Q., Cao, X.F., Zhao, L., Wang, J., Gao, Z., Wang, M.C. et al. (2016) The importance of neutral and niche processes for bacterial community assembly differs between habitat generalists and specialists. FEMS Microbiology Ecology, 92, fiw174.
Logares, R., Lindström, E.S., Langenheder, S., Logue, J.B., Paterson, H., Laybourn-Parry, J. et al. (2013) Biogeography of bacterial communities exposed to progressive long-term environmental change. The ISME Journal, 7, 937-948.
Lozupone, C.A. & Knight, R. (2007) Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences of the United States of America, 104, 11436-11440.
Maestre, F.T., Quero, J.L., Gotelli, N.J., Escudero, A., Ochoa, V., Delgado-Baquerizo, M. et al. (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science, 335, 214-218.
Maestre, F.T., Eldridge, D.J., Soliveres, S., Kéfi, S., Delgado-Baquerizo, M., Bowker, M.A. et al. (2016) Structure and functioning of dryland ecosystems in a changing world. Annual Review of Ecology, Evolution, and Systematics, 47, 215-237.
Malard, L.A., Anwar, M.Z., Jacobsen, C.S. & Pearce, D.A. (2019) Biogeographical patterns in soil bacterial communities across the Arctic region. FEMS Microbiology Ecology, 95, fiz128.
Moin, N.S., Nelson, K.A., Bush, A. & Bernhard, A.E. (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Applied and Environmental Microbiology, 75, 7461-7468.
Mosier, A.C. & Francis, C.A. (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environmental Microbiology, 10, 3002-3016.
Nicol, G.W., Tscherko, D., Embley, T.M. & Prosser, J.I. (2005) Primary succession of soil Crenarchaeota across a receding glacier foreland. Environmental Microbiology, 7, 337-347.
Ochoa-Hueso, R., Eldridge, D.J., Delgado-Baquerizo, M., Soliveres, S., Bowker, M.A., Gross, N. et al. (2018) Soil fungal abundance and plant functional traits drive fertile Island formation in global drylands. Journal of Ecology, 106, 242-253.
Offre, P., Spang, A. & Schleper, C. (2013) Archaea in biogeochemical cycles. Annual Review of Microbiology, 67, 437-457.
Oren, A. (1994) The ecology of the extremely halophilic archaea. FEMS Microbiology Reviews, 13, 415-439.
Oren, A. (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems, 4, 2.
Oren, A. (2013) Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Frontiers in Microbiology, 4, 315.
Pandit, S.N., Kolasa, J. & Cottenie, K. (2009) Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology, 90, 2253-2262.
Pester, M., Schleper, C. & Wagner, M. (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Current Opinion in Microbiology, 14, 300-306.
Pointing, S.B. & Belnap, J. (2012) Microbial colonization and controls in dryland systems. Nature Reviews Microbiology, 10, 551-562.
Price, M.N., Dehal, P.S. & Arkin, A.P. (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One, 5, e9490.
Rath, K.M., Fierer, N., Murphy, D.V. & Rousk, J. (2019) Linking bacterial community composition to soil salinity along environmental gradients. The ISME Journal, 13, 836-846.
Shi, Y., Adams, J.M., Ni, Y.Y., Yang, T., Jing, X., Chen, L.T. et al. (2016) The biogeography of soil archaeal communities on the eastern Tibetan plateau. Scientific Reports, 6, 38893.
Simon, H.M., Dodsworth, J.A. & Goodman, R.M. (2000) Crenarchaeota colonize terrestrial plant roots. Environmental Microbiology, 2, 495-505.
Simon, H.M., Jahn, C.E., Bergerud, L.T., Sliwinski, M.K., Weimer, P.J., Willis, D.K. et al. (2005) Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots. Applied and Environmental Microbiology, 71, 4751-4760.
Sliwinski, M.K. & Goodman, R.M. (2004) Comparison of crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Applied and Environmental Microbiology, 70, 1821-1826.
Stegen, J.C., Lin, X.J., Konopka, A.E. & Fredrickson, J.K. (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. The ISME Journal, 6, 1653-1664.
Stegen, J.C., Lin, X.J., Fredrickson, J.K., Chen, X.Y., Kennedy, D.W., Murray, C.J. et al. (2013) Quantifying community assembly processes and identifying features that impose them. The ISME Journal, 7, 2069-2079.
Stegen, J.C., Lin, X.J., Fredrickson, J.K. & Konopka, A.E. (2015) Estimating and mapping ecological processes influencing microbial community assembly. Frontiers in Microbiology, 6, 370.
Subramanian, B., Gao, S.H., Lercher, M.J., Hu, S.N. & Chen, W.-H. (2019) Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Research, 47, 270-275.
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.
Trivedi, C., Reich, P.B., Maestre, F.T., Hu, H.-W., Singh, B.K. & Delgado-Baquerizo, M. (2019) Plant-driven niche differentiation of ammonia-oxidizing bacteria and archaea in global drylands. The ISME Journal, 13, 2727-2736.
Valentine, D.L. (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Reviews Microbiology, 5, 316-323.
Walsh, D.A., Papke, R.T. & Doolittle, W.F. (2005) Archaeal diversity along a soil salinity gradient prone to disturbance. Environmental Microbiology, 7, 1655-1666.
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., van der Putten, W.H. & Wall, D.H. (2004) Ecological linkages between aboveground and belowground biota. Science, 304, 1629-1633.
Zhang, Y.H., Loreau, M., He, N.P., Wang, J.B., Pan, Q.M., Bai, Y.F. et al. (2018) Climate variability decreases species richness and community stability in a temperate grassland. Oecologia, 188, 183-192.
Zhang, K.P., Shi, Y., Cui, X.Q., Yue, P., Li, K.H., Liu, X.J. et al. (2019) Salinity is a key determinant for soil microbial communities in a desert ecosystem. mSystems, 4, e00225-18.

Auteurs

Weigang Hu (W)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Qingqing Hou (Q)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Manuel Delgado-Baquerizo (M)

Laboratorio de Biodiversidad y Funcionamiento Ecosistemico. Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.
Unidad Asociada CSIC-UPO (BioFun). Universidad Pablo de Olavide, Sevilla, Spain.

James C Stegen (JC)

Ecosystem Science Team, Pacific Northwest National Laboratory, Richland, Washington, USA.

Qiajun Du (Q)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Longwei Dong (L)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Mingfei Ji (M)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Yuan Sun (Y)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Shuran Yao (S)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Haiyang Gong (H)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Junlan Xiong (J)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Rui Xia (R)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Jiayuan Liu (J)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Muhammad Aqeel (M)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Muhammad Adnan Akram (MA)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.
School of Economics, Lanzhou University, Lanzhou, China.

Jinzhi Ran (J)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

Jianming Deng (J)

State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou, China.

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