Microbial Data Synthesis and Meta-analysis for the Biodiversity Exploratories
Final Report Abstract
MicroSYSteM was designed as a separate synthesis and meta-analysis project within the Biodiversity Exploratories to focus on soil microbial diversity. For most soil bacteria, the actual habitat adaptations have largely remained unresolved due to the fact that only about 18,000 of the estimated up to 10^9 bacterial species have been described to date. To determine niche spaces of a large number of 4154 different types of Acidobacteria as a model group, we used the occurrence patterns of bacterial sequence types along gradients of 41 environmental variables and employed a niche modeling approach that yielded values for optimum activity for each variable. Although the evolution of habitat adaptation was mainly cladogenic, it was disrupted by recurrent events of convergent evolution that resulted in frequent habitat switching within individual clades of Acidobacteria. Our findings indicate that the high diversity of soil acidobacterial communities is largely sustained by differential habitat adaptation even at the level of closely related species. One of the largest knowledge gaps to date is the lack of understanding of the link between microbial community composition and ecosystem processes. It is unclear how changes in the relative composition of microbial communities can be predicted to affect soil processes. Since only a fraction of soil bacteria is active and thus contributes to ecosystem process, we utilized the ratio of the 16S rRNA gene transcripts to 16S rRNA genes (the rRNA/rDNA ratio) as an indicator of cellular ribosome content which in turn reflects potential activity. It was necessary to develop a novel statistical procedure to distinguish reliable values from those that were false positive due stochastic sequencing noise. Approximately 1% of the bacterial richness at sequence variant level was classified to be active. Statistical modeling of response variables that describe key ecosystem functions like respiration or biomass degradation, revealed that the counts of active taxa had the strongest explanatory power for soil respiration and enzymatic activities related to the carbon cycle (glucosidase, xylosidase and chitinase), whereas community composition (richness of rDNA sequences) had only low predictive power. Interactions between microorganisms in densely populated habitats such as soils likely represent important drivers of microbial community structure and function. Improved network analysis was used to construct networks for 206,849 bacterial and 19,791 fungal sequence variants in all 300 Experimental Plots of the Exploratories and to identify potential interactions between microorganisms and the specific microbial keystone sequence variants in different types of soils. Notably, the keystone sequence variants often correlated with active sequence variants (as identified by their high rRNA/rDNA ratio), thereby providing independent evidence for a key role of these sequence variants in the interaction network because of their specific activity. Since co-occurrence may only reflect similar responses towards environmental pressures rather than direct interaction, however, we also developed a novel framework for the analysis of interactions as a function of differences in environmental conditions. This framework is based on a generalized Lotka-Volterra approach and can accomodate large datasets from the Exploratories.
Publications
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(2015) Spatial interaction of archaeal ammonia-oxidizers and nitrite-oxidizing bacteria in an unfertilized grassland soil. Front Microbiol 6, 1567
Stempfhuber B, Richter-Heitmann T, Regan KM, Kölbl A, Wüst P, Marhan S, Sikorski J, Overmann J, Friedrich MW, Kandeler E, Schloter M
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(2016) Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature 536, 456-459
Soliveres S, van der Plas F, Manning P, Prati D, Gossner MM, Renner SC, Alt F, Arndt H, Baumgartner V, Binkenstein J, Birkhofer K, Blaser S, Blüthgen N, Boch S, Böhm S, Börschig C, Buscot F, Diekötter T, Heinze J, Hölzel N, Jung K, Klaus VH, Kleinebecker T, Klemmer S, Krauss J, Lange M, Morris K, Müller J, Oelmann Y, Overmann J, Pašalić E, Rillig MC, Schaefer HM, Schloter M, Schmitt B, Schöning I, Schrumpf M, Sikorski J, Socher SA, Solly EF, Sonnemann I, Sorkau E, Steckel J, Steffan-Dewenter I, Stempfhuber B, Tschapka M, Türke M, Venter P, Weiner CN, Weisser WW, Werner M, Westphal C, Wilcke W, Wolters V, Wubet T, Wurst S, Fischer M, Allan E
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(2016) Estimates of the bacterial ribosome content and diversity in soils are significantly affected by different nucleic acid extraction methods. Appl Environ Microbiol 82, 2595-2607
Wüst PK, Nacke H, Kaiser K, Marhan S, Sikorski J, Kandeler E, Daniel R, Overmann J
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(2016) Land-use intensification causes homogenization of grassland communities across trophic levels. Nature 540, 266-269
Gossner MM, Lewinsohn T, Kahl T, Grassein F, Boch S, Prati D, Birkhofer K, Renner SC, Sikorski J, Arndt H, Baumgartner V, Blaser S, Blüthgen N, Börschig C, Buscot F, Diekötter T, Jorge LR, Jung K, Keyel AC, Klein A-M, Klemmer S, Krauss J, Lange M, Müller J, Overmann J, Pasalic E, Penone C, Perovic D, Purschke O, Schall P, Socher SA, Sonnemann I, Tschapka M, Tscharntke T, Türke M, Venter PC, Weiner CN, Werner M, Wolters V, Wurst S, Westphal C, Wubet T, Fischer M, Weisser WW, Allan E
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(2016) Locally rare species influence grassland ecosystem multifunctionality. Phil Trans R Soc B 371, 20150269
Soliveres S, Manning P, Prati D, Gossner MM, Alt F, Arndt H, Baumgartner V, Binkenstein J, Birkhofer K, Blaser S, Blüthgen N, Boch S, Böhm S, Börschig C, Buscot F, Diekötter T, Heinze J, Hölzel N, Jung K, Klaus VH, Klein A-M, Kleinebecker T, Klemmer S, Krauss J, Lange M, Morris EK, Müller J, Oelmann Y, Overmann J, Pašalić E, Renner SC, Rillig MC, Schäfer M, Schloter M, Schmitt B, Schöning I, Schrumpf M, Sikorski J, Socher SA, Solly EF, Sonnemann I, Sorkau E, Steckel J, Steffen-Dewenter I, Stempfhuber B, Tschapka M, Türke M, Venter P, Weiner CN, Weisser WW, Werner M, Westphal C, Wilcke W, Wolters V, Wubet T, Wurst S, Fischer M, Allan E
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(2017) Function of bacterial community dynamics in the formation of cadaveric semiochemicals during in situ carcass decomposition. Environ Microbiol 19, 3310-3322
Pascual J, von Hoermann C, Rottler-Hoermann A-M, Nevo O, Geppert A, Sikorski J, Huber KJ, Steiger S, Ayasse M, Overmann J
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(2017) Inferring interactions in complex microbial communities from nucleotide sequence data and environmental parameters. PLoS One 12, e0173765
Shang Y, Sikorski J, Bonkowski M, Fiore-Donno A-M, Kandeler E, Boeddinghaus R, Marhan S, Solly E, Schrumpf M, Schöning I, Tesfaye W, Buscot F, Overmann J
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(2018) The impact of even-aged and uneven-aged forest management on regional biodiversity of multiple taxa in European beech forests. J Appl Ecol 55, 267-278
Schall P, Gossner MM, Heinrichs S, Fischer M, Boch S, Prati D, Jung K, Baumgartner V, Blaser S, Böhm S, Buscot F, Daniel R, Goldmann K, Kaiser K, Kahl T, Lange M, Müller J, Overmann J, Pašalić E, Renner S, Schulze E-D, Sikorski J, Tschapka M, Türke M, Weisser WW, Wemheuer B, Wubet T, Ammer C
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(2019) Functional traits and spatio-temporal structure of a major group of soil protists (Rhizaria: Cercozoa) in a temperate grassland. Frontiers in Microbiology 10: 1332
Fiore-Donno AM, Richter-Heitmann T, Degrune F, Dumack K, Regan KM, Mahran S, Boeddinghaus RS, Rillig MC, Friedrich MW, Kandeler E, Bonkowski M
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(2020) Bacterial colonization of reactive minerals in grassland soils is selective and highly dynamic. Environ Microbiol 22, 917-933
Vieira S, Sikorski J, Gebala A, Boeddinghaus R, Marhan S, Rennert T, Kandeler E, Overmann J
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(2020) Can multi-taxa diversity in European beech forest landscapes be increased by combining different management systems? J Appl Ecol. 57, 1363-1375
Schall P, Heinrichs S, Ammer C, Ayasse M, Boch S, Buscot F, Fischer M, Goldmann K, Overmann J, Schulze E-D, Sikorski J, Weisser W, Wubet T, Gossner MM
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(2020) Direct and indirect effects of forest management on tree-hole inhabiting aquatic organisms and their functional traits. Sci Total Environ 704, 135418
Petermann JS, Roberts AL, Hemmerling C, Bajerski F, Pascual J, Overmann J, Weisser W, Ruess L, Gossner M
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(2020) Land-use intensity alters networks between biodiversity, ecosystem functions, and services. Proc Natl Acad Sci USA 117, 28140-28149
Felipe-Lucia MR, Soliveres S, Penone C, Fischer M, Ammer C, Boch S, Boeddinghaus RS, Bonkowski M, Buscot F, Fiore-Donno AM, Frank K, Goldmann K, Gossner MM, Hölzel N, Jochum M, Kandeler E, Klaus VH, Kleinebecker T, Leimer S, Manning P, Oelmann Y, Saiz H, Schall P, Schloter M, Schöning I, Schrumpf M, Solly EF, Stempfhuber B, Weisser WW, Wilcke W, Wubet T, Allan E
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(2020) Spatiotemporal variation of arbuscular mycorrhizal fungal communities in a homogeneous grassland. Environmental Microbiology 22, 873–888
Goldmann K, Boeddinghaus RS, Klemmer S, Regan KM, Heintz-Buschart A, Klaus VH, Fischer M, Prati D, Piepho HP, Berner D, Marhan S, Kandeler E, Buscot F, Wubet T
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(2021) Contrasting responses of above- and belowground diversity to multiple components of land-use intensity. Nature Comm 12: 3918
Le Provost G, Thiele J, Westphal C, Penone C, Allan E, Neyret M, van der Plas F, Ayasse M, Bardgett RD, Birkhofer K, Boch S, Bonkowski M, Buscot F, Feldhaar H, Gaulton R, Goldmann K, Gossner MM, Klaus VH, Kleinebecker T, Krauss J, Renner S, Scherreiks P, Sikorski J, Baulechner D, Blüthgen N, Bolliger R, Börschig C, Busch V, Chisté M, Fiore-Donno AM, Fischer M, Arndt H, Hölzel N, John K, Jung K, Lange M, Marzini C, Overmann J, Paŝalić E, Perović DJ, Prati D, Schäfer D, Schöning I, Schrumpf M, Sonnemann I, Steffan-Dewenter I, Tschapka M, Türke M, Vogt J, Wehner K, Weiner C, Weisser W, Wells W, Werner M, Wolters V, Wubet T, Wurst S, Zaytev A, Manning P
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(2021) The Mineralosphere – Interactive zone of microbial colonization and carbon use in grassland soils. Biol Fertil Soils 57, 587-601
Boeddinghaus RS, Marhan S, Gebala A, Haslwimmer H, Vieira S, Sikorski J, Overmann J, Soares M, Rousk J, Rennert T, Kandeler E
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(2022) Biological soil crust from mesic forests promote a specific bacteria community. Front Microbiol
Glaser K, Albrecht M, Baumann K, Overmann J, Sikorski J
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(2022) The evolution of ecological diversity in Acidobacteria. Front Microbiol
Sikorski J, Baumgartner V, Birkhofer K, Boeddinghaus RS, Bunk B, Fischer M, Fösel B, Friedrich MW, Göker M, Hölzel N, Huang S, Huber KJ, Kandeler E, Klaus VH, Kleinebecker T, Marhan S, von Mering C, Oelmann Y, Prati D, Regan KM, Richter-Heitmann T, Rodrigues JFM, Schmitt B, Schöning I, Schrumpf M, Schurig E, Solly EF, Wolters V, Overmann J