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Life and death in the soil microbiome: how ecological processes influence biogeochemistry

Nature Reviews Microbiology volume 20, pages 415–430 (2022)Cite this article

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Abstract

Soil microorganisms shape global element cycles in life and death. Living soil microorganisms are a major engine of terrestrial biogeochemistry, driving the turnover of soil organic matter — Earth’s largest terrestrial carbon pool and the primary source of plant nutrients. Their metabolic functions are influenced by ecological interactions with other soil microbial populations, soil fauna and plants, and the surrounding soil environment. Remnants of dead microbial cells serve as fuel for these biogeochemical engines because their chemical constituents persist as soil organic matter. This non-living microbial biomass accretes over time in soil, forming one of the largest pools of organic matter on the planet. In this Review, we discuss how the biogeochemical cycling of organic matter depends on both living and dead soil microorganisms, their functional traits, and their interactions with the soil matrix and other organisms. With recent omics advances, many of the traits that frame microbial population dynamics and their ecophysiological adaptations can be deciphered directly from assembled genomes or patterns of gene or protein expression. Thus, it is now possible to leverage a trait-based understanding of microbial life and death within improved biogeochemical models and to better predict ecosystem functioning under new climate regimes.

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Fig. 1: Composition of the soil microbiome and its role in organic matter cycling in different soil habitats.
Fig. 2: Microbial succession and organic matter formation in the rhizosphere.
Fig. 3: Biotic interactions and density-dependent processes in the soil profile.
Fig. 4: Mechanisms of microbial mortality and theorized effects on the fate of microbial necromass.

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References

  1. Guerra, C. A. et al. Tracking, targeting, and conserving soil biodiversity. Science 371, 239–241 (2021).

    Article  CAS  PubMed  Google Scholar 

  2. Orgiazzi, A. et al. Global Soil Biodiversity Atlas (European Commission, Publications Office of the European Union, 2016).

  3. Tecon, R. & Or, D. Biophysical processes supporting the diversity of microbial life in soil. FEMS Microbiol. Rev. 41, 599–623 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Williamson, K. E., Fuhrmann, J. J., Wommack, K. E. & Radosevich, M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu. Rev. Virol. 4, 201–219 (2017). This Review provides a comprehensive overview of methods and technologies used to study soil viruses alongside a guide of metrics describing soil viruses across diverse soil ecosystems.

    Article  CAS  PubMed  Google Scholar 

  5. Stefan, G., Cornelia, B., Jörg, R. & Michael, B. Soil water availability strongly alters the community composition of soil protists. Pedobiologia 57, 205–213 (2014).

    Article  Google Scholar 

  6. Leake, J. et al. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 1016–1045 (2004).

    Article  Google Scholar 

  7. Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018). This study compiled metagenomic and metabarcoding data from 189 sites to demonstrate global patterns in the structure and function of soil microbial communities as well as the widespread prevalence of bacterial–fungal antagonism as an important structuring force of microbial communities.

    Article  CAS  PubMed  Google Scholar 

  8. He, L. et al. Global biogeography of fungal and bacterial biomass carbon in topsoil. Soil Biol. Biochem. 151, 108024 (2020).

    Article  CAS  Google Scholar 

  9. Bach, E. M., Williams, R. J., Hargreaves, S. K., Yang, F. & Hofmockel, K. S. Greatest soil microbial diversity found in micro-habitats. Soil Biol. Biochem. 118, 217–226 (2018).

    Article  CAS  Google Scholar 

  10. Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).

    Article  CAS  PubMed  Google Scholar 

  11. Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017).

    Article  CAS  PubMed  Google Scholar 

  12. Delgado-Baquerizo, M. et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat. Ecol. Evol. 4, 210–220 (2020).

    Article  PubMed  Google Scholar 

  13. Crowther, T. W. et al. The global soil community and its influence on biogeochemistry. Science 365, eaav0550 (2019).

    Article  CAS  PubMed  Google Scholar 

  14. Liang, C., Amelung, W., Lehmann, J. & Kästner, M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob. Change Biol. 25, 3578–3590 (2019). This article estimates that more than 50% of SOM may be derived from microbial necromass in grassland and agricultural ecosystems based on extrapolations from amino sugar biomarker data.

    Article  Google Scholar 

  15. Angst, G., Mueller, K. E., Nierop, K. G. J. & Simpson, M. J. Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter. Soil Biol. Biochem. 156, 108189 (2021).

    Article  CAS  Google Scholar 

  16. Ludwig, M. et al. Microbial contribution to SOM quantity and quality in density fractions of temperate arable soils. Soil Biol. Biochem. 81, 311–322 (2015). This study uses lipid biomarkers to estimate that at least 50% of SOM may be derived from microbial necromass.

    Article  CAS  Google Scholar 

  17. Simpson, A. J., Simpson, M. J., Smith, E. & Kelleher, B. P. Microbially derived inputs to soil organic matter: are current estimates too low? Environ. Sci. Technol. 41, 8070–8076 (2007).

    Article  CAS  PubMed  Google Scholar 

  18. Blazewicz, S. J. et al. Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil. ISME J. 14, 1520–1532 (2020). This study used quantitative stable isotope probing to calculate growth and mortality rates of bacteria following the rewetting of a dry Mediterranean soil, and demonstrated that bacterial growth was density independent whereas bacterial mortality was density dependent.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Vieira, S. et al. Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands. ISME J. 14, 463–475 (2020).

    Article  CAS  PubMed  Google Scholar 

  20. Nuccio, E. E. et al. Niche differentiation is spatially and temporally regulated in the rhizosphere. ISME J. 14, 999–1014 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Shi, S. et al. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6, e00746 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Bastian, F., Bouziri, L., Nicolardot, B. & Ranjard, L. Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biol. Biochem. 41, 262–275 (2009).

    Article  CAS  Google Scholar 

  23. Whitman, T. et al. Microbial community assembly differs across minerals in a rhizosphere microcosm. Environ. Microbiol. 20, 4444–4460 (2018).

    Article  CAS  PubMed  Google Scholar 

  24. Maynard, D. S., Crowther, T. W. & Bradford, M. A. Fungal interactions reduce carbon use efficiency. Ecol. Lett. 20, 1034–1042 (2017). This study demonstrated that antagonistic interactions between wood-decay fungi can reduce CUE of the fungal community.

    Article  PubMed  Google Scholar 

  25. Crowther, T. W. et al. Environmental stress response limits microbial necromass contributions to soil organic carbon. Soil Biol. Biochem. 85, 153–161 (2015).

    Article  CAS  Google Scholar 

  26. Hu, Y., Zheng, Q., Noll, L., Zhang, S. & Wanek, W. Direct measurement of the in situ decomposition of microbial-derived soil organic matter. Soil Biol. Biochem. 141, 107660 (2020).

    Article  CAS  Google Scholar 

  27. Fernandez, C. W., Langley, J. A., Chapman, S., McCormack, M. L. & Koide, R. T. The decomposition of ectomycorrhizal fungal necromass. Soil Biol. Biochem. 93, 38–49 (2016). This review article summarizes how the stoichiometry, morphology and chemistry of microbial necromass affects its decomposition rate in soil.

    Article  CAS  Google Scholar 

  28. Buckeridge, K. M. et al. Sticky dead microbes: rapid abiotic retention of microbial necromass in soil. Soil Biol. Biochem. 149, 107929 (2020).

    Article  CAS  Google Scholar 

  29. Creamer, C. A. et al. Mineralogy dictates the initial mechanism of microbial necromass association. Geochim. Cosmochim. Acta 260, 161–176 (2019). This study used Raman microspectroscopy and 13C-labelled necromass to demonstrate that different mineral types retained microbial necromass through different mechanisms and with different strengths.

    Article  CAS  Google Scholar 

  30. Schurig, C. et al. Microbial cell-envelope fragments and the formation of soil organic matter: a case study from a glacier forefield. Biogeochemistry 113, 595–612 (2013).

    Article  CAS  Google Scholar 

  31. Kopittke, P. M. et al. Nitrogen-rich microbial products provide new organo-mineral associations for the stabilization of soil organic matter. Glob. Change Biol. 24, 1762–1770 (2018).

    Article  Google Scholar 

  32. Miltner, A., Bombach, P., Schmidt-Brücken, B. & Kästner, M. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2012).

    Article  CAS  Google Scholar 

  33. Kleber, M. et al. Dynamic interactions at the mineral–organic matter interface. Nat. Rev. Earth Environ. 2, 402–421 (2021).

    Article  Google Scholar 

  34. Blagodatskaya, E. & Kuzyakov, Y. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol. Biochem. 67, 192–211 (2013).

    Article  CAS  Google Scholar 

  35. Or, D., Smets, B. F., Wraith, J. M., Dechesne, A. & Friedman, S. P. Physical constraints affecting bacterial habitats and activity in unsaturated porous media–a review. Adv. Water Resour. 30, 1505–1527 (2007).

    Article  Google Scholar 

  36. Kuzyakov, Y. & Blagodatskaya, E. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199 (2015).

    Article  CAS  Google Scholar 

  37. Finzi, A. C. et al. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob. Change Biol. 21, 2082–2094 (2015).

    Article  Google Scholar 

  38. Yuan, M. M. et al. Fungal-bacterial cooccurrence patterns differ between arbuscular mycorrhizal fungi and nonmycorrhizal fungi across soil niches. mBio 12, e03509-20 (2015).

    Article  Google Scholar 

  39. Zhang, L. & Lueders, T. Micropredator niche differentiation between bulk soil and rhizosphere of an agricultural soil depends on bacterial prey. FEMS Microbiol. Ecol. 93, fix103 (2017).

    CAS  Google Scholar 

  40. Sokol, N. W. & Bradford, M. A. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat. Geosci. 12, 46–53 (2019).

    Article  CAS  Google Scholar 

  41. Kallenbach, C. M., Frey, S. D. & Grandy, A. S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7, 13630 (2016). This study used artificial soils to provide empirical evidence that SOM can be entirely microbially derived, and also demonstrated a positive relationship between CUE and SOM formation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wood, J. L., Tang, C. & Franks, A. E. Competitive traits are more important than stress-tolerance traits in a cadmium-contaminated rhizosphere: a role for trait theory in microbial ecology. Front. Microbiol. 9, 121 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Violle, C. et al. Let the concept of trait be functional! Oikos 116, 882–892 (2007).

    Article  Google Scholar 

  44. Madin, J. S. et al. A synthesis of bacterial and archaeal phenotypic trait data. Sci. Data 7, 170 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Shaffer, M. et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 48, 8883–8900 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Brown, C. T., Olm, M. R., Thomas, B. C. & Banfield, J. F. Measurement of bacterial replication rates in microbial communities. Nat. Biotechnol. 34, 1256–1263 (2016). This study developed an algorithm, iRep, that uses draft-quality genome sequences and single time-point metagenome sequencing to infer microbial population replication rates.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Nayfach, S. & Pollard, K. S. Average genome size estimation improves comparative metagenomics and sheds light on the functional ecology of the human microbiome. Genome Biol. 16, 51 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Leff, J. W. et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc. Natl Acad. Sci. USA 112, 10967–10972 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Vieira-Silva, S. & Rocha, E. P. C. The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet. 6, e1000808 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Hasby, F. A., Barbi, F., Manzoni, S. & Lindahl, B. D. Transcriptomic markers of fungal growth, respiration and carbon-use efficiency. FEMS Microbiol. Lett. 368, fnab100 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Maillard, F., Schilling, J., Andrews, E., Schreiner, K. M. & Kennedy, P. Functional convergence in the decomposition of fungal necromass in soil and wood. FEMS Microbiol. Ecol. 96, fiz209 (2020).

    Article  CAS  PubMed  Google Scholar 

  52. Clemmensen, K. E. et al. Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. N. Phytol. 205, 1525–1536 (2015).

    Article  CAS  Google Scholar 

  53. Olivelli, M. S. et al. Unraveling mechanisms behind biomass–clay interactions using comprehensive multiphase nuclear magnetic resonance (NMR) Spectroscopy. ACS Earth Space Chem. 4, 2061–2072 (2020).

    Article  CAS  Google Scholar 

  54. Achtenhagen, J., Goebel, M.-O., Miltner, A., Woche, S. K. & Kästner, M. Bacterial impact on the wetting properties of soil minerals. Biogeochemistry 122, 269–280 (2015).

    Article  CAS  Google Scholar 

  55. Lehmann, J. et al. Persistence of soil organic carbon caused by functional complexity. Nat. Geosci. 13, 529–534 (2020).

    Article  CAS  Google Scholar 

  56. Ahmed, E. & Holmström, S. J. M. Microbe–mineral interactions: The impact of surface attachment on mineral weathering and element selectivity by microorganisms. Chem. Geol. 403, 13–23 (2015).

    Article  CAS  Google Scholar 

  57. Chenu, C. Clay- or sand-polysaccharide associations as models for the interface between micro-organisms and soil: water related properties and microstructure. Geoderma 56, 143–156 (1993).

    Article  CAS  Google Scholar 

  58. Sher, Y. et al. Microbial extracellular polysaccharide production and aggregate stability controlled by switchgrass (Panicum virgatum) root biomass and soil water potential. Soil Biol. Biochem. 143, 107742 (2020).

    Article  CAS  Google Scholar 

  59. Lybrand, R. A. et al. A coupled microscopy approach to assess the nano-landscape of weathering. Sci. Rep. 9, 5377 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Prommer, J. et al. Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity. Glob. Change Biol. 26, 669–681 (2020).

    Article  Google Scholar 

  61. Cotrufo, M. F., Wallenstein, M. D., Boot, C. M., Denef, K. & Paul, E. The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob. Change Biol. 19, 988–995 (2013).

    Article  Google Scholar 

  62. Liang, C., Schimel, J. P. & Jastrow, J. D. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol. 2, 17105 (2017).

    Article  CAS  PubMed  Google Scholar 

  63. Geyer, K. M., Kyker-Snowman, E., Grandy, A. S. & Frey, S. D. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127, 173–188 (2016).

    Article  CAS  Google Scholar 

  64. Kallenbach, C. M., Grandy, A. S., Frey, S. D. & Diefendorf, A. F. Microbial physiology and necromass regulate agricultural soil carbon accumulation. Soil Biol. Biochem. 91, 279–290 (2015).

    Article  CAS  Google Scholar 

  65. Buckeridge, K. M. et al. Environmental and microbial controls on microbial necromass recycling, an important precursor for soil carbon stabilization. Commun. Earth Env. 1, 36 (2020).

    Article  Google Scholar 

  66. Saifuddin, M., Bhatnagar, J. M., Segrè, D. & Finzi, A. C. Microbial carbon use efficiency predicted from genome-scale metabolic models. Nat. Commun. 10, 3568 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).

    Article  PubMed  Google Scholar 

  68. Mason‐Jones, K., Banfield, C. C. & Dippold, M. A. Compound-specific 13C stable isotope probing confirms synthesis of polyhydroxybutyrate by soil bacteria. Rapid Commun. Mass. Spectrom. 33, 795–802 (2019).

    Article  PubMed  CAS  Google Scholar 

  69. Bååth, E. The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microb. Ecol. 45, 373–383 (2003).

    Article  PubMed  CAS  Google Scholar 

  70. Slessarev, E. W. et al. Cellular and extracellular C contributions to respiration after wetting dry soil. Biogeochemistry 147, 307–324 (2020).

    Article  CAS  Google Scholar 

  71. Slessarev, E. W. & Schimel, J. P. Partitioning sources of CO2 emission after soil wetting using high-resolution observations and minimal models. Soil Biol. Biochem. 143, 107753 (2020).

    Article  CAS  Google Scholar 

  72. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

    Article  CAS  PubMed  Google Scholar 

  73. Brangarí, A. C., Manzoni, S. & Rousk, J. A soil microbial model to analyze decoupled microbial growth and respiration during soil drying and rewetting. Soil Biol. Biochem. 148, 107871 (2020).

    Article  CAS  Google Scholar 

  74. Zha, J. & Zhuang, Q. Microbial dormancy and its impacts on northern temperate and boreal terrestrial ecosystem carbon budget. Biogeosciences 17, 4591–4610 (2020).

    Article  CAS  Google Scholar 

  75. Anderson, T.-H. Microbial eco-physiological indicators to asses soil quality. Agric. Ecosyst. Environ. 98, 285–293 (2003).

    Article  Google Scholar 

  76. Geyer, K., Schnecker, J., Grandy, A. S., Richter, A. & Frey, S. Assessing microbial residues in soil as a potential carbon sink and moderator of carbon use efficiency. Biogeochemistry 151, 237–249 (2020).

    Article  CAS  Google Scholar 

  77. Sepehrnia, N. et al. Transport, retention, and release of Escherichia coli and Rhodococcus erythropolis through dry natural soils as affected by water repellency. Sci. Total Environ. 694, 133666 (2019).

    Article  CAS  PubMed  Google Scholar 

  78. Boeddinghaus, R. S. et al. The mineralosphere — interactive zone of microbial colonization and carbon use in grassland soils. Biol. Fertil. Soils 57, 587–601 (2021).

    Article  CAS  Google Scholar 

  79. Vieira, S. et al. Bacterial colonization of minerals in grassland soils is selective and highly dynamic. Environ. Microbiol. 22, 917–933 (2020).

    Article  CAS  PubMed  Google Scholar 

  80. Ma, T. et al. Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nat. Commun. 9, 3480 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Blazewicz, S. J., Schwartz, E. & Firestone, M. K. Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95, 1162–1172 (2014).

    Article  PubMed  Google Scholar 

  82. Ceja-Navarro, J. A. et al. Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop. Microbiome 9, 96 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Starr, E. P., Nuccio, E. E., Pett-Ridge, J., Banfield, J. F. & Firestone, M. K. Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil. Proc. Natl Acad. Sci. USA 116, 25900–25908 (2019). This comprehensive study of RNA viruses detectable in a grassland soil showed how these viruses are shaped by the presence of plant roots and litter.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Shi, S. et al. The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol. Lett. 19, 926–936 (2016).

    Article  PubMed  Google Scholar 

  85. Yan, Y., Kuramae, E. E., de Hollander, M., Klinkhamer, P. G. L. & van Veen, J. A. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. ISME J. 11, 56–66 (2017).

    Article  PubMed  Google Scholar 

  86. Zhalnina, K. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3, 470 (2018).

    Article  CAS  PubMed  Google Scholar 

  87. Pett-Ridge, J. et al. in Rhizosphere Biology: Interactions Between Microbes and Plants (eds Gupta, V. V. S. R. & Sharma, A. K.) 51–73 (Springer, 2021).

  88. Poll, C., Marhan, S., Ingwersen, J. & Kandeler, E. Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biol. Biochem. 40, 1306–1321 (2008).

    Article  CAS  Google Scholar 

  89. Buchkowski, R. W., Bradford, M. A., Grandy, A. S., Schmitz, O. J. & Wieder, W. R. Applying population and community ecology theory to advance understanding of belowground biogeochemistry. Ecol. Lett. 20, 231–245 (2017).

    Article  PubMed  Google Scholar 

  90. Erktan, A., Or, D. & Scheu, S. The physical structure of soil: determinant and consequence of trophic interactions. Soil Biol. Biochem. 148, 107876 (2020).

    Article  CAS  Google Scholar 

  91. Roesch, L. F. W. et al. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283–290 (2007).

    Article  CAS  PubMed  Google Scholar 

  92. Carson, J. K. et al. Low pore connectivity increases bacterial diversity in soil. Appl. Environ. Microbiol. 76, 3936–3942 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Raynaud, X. & Nunan, N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE 9, e87217 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Ekelund, F., Rønn, R. & Christensen, S. Distribution with depth of protozoa, bacteria and fungi in soil profiles from three Danish forest sites. Soil Biol. Biochem. 33, 475–481 (2001).

    Article  CAS  Google Scholar 

  95. Sharrar, A. M. et al. Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. mBio 11, e00416-20 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Georgiou, K., Abramoff, R. Z., Harte, J., Riley, W. J. & Torn, M. S. Microbial community-level regulation explains soil carbon responses to long-term litter manipulations. Nat. Commun. 8, 1223 (2017). This modelling study demonstrated that including a density-dependent microbial mortality term can reduce the oscillatory behaviour of soil carbon models.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Thakur, M. P. & Geisen, S. Trophic regulations of the soil microbiome. Trends Microbiol. 27, 771–780 (2019).

    Article  CAS  PubMed  Google Scholar 

  98. Fanin, N. et al. The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biol. Biochem. 128, 111–114 (2019).

    Article  CAS  Google Scholar 

  99. Wang, W. et al. Predatory Myxococcales are widely distributed in and closely correlated with the bacterial community structure of agricultural land. Appl. Soil Ecol. 146, 103365 (2020).

    Article  Google Scholar 

  100. Hungate, B. A. et al. The functional significance of bacterial predators. mBio 12, e00466-21 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Jover, L. F., Effler, T. C., Buchan, A., Wilhelm, S. W. & Weitz, J. S. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12, 519–528 (2014).

    Article  CAS  PubMed  Google Scholar 

  102. Emerson, J. B. et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3, 870–880 (2018). This study identified novel viral genomes from metagenomes and linked many of these viruses in silico to bacterial hosts and carbon metabolisms across the spatial gradient of permafrost thaw.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Ren, D., Madsen, J. S., Sørensen, S. J. & Burmølle, M. High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J. 9, 81–89 (2015).

    Article  CAS  PubMed  Google Scholar 

  104. Lee, K. W. K. et al. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 8, 894–907 (2014).

    Article  CAS  PubMed  Google Scholar 

  105. Witzgall, K. et al. Particulate organic matter as a functional soil component for persistent soil organic carbon. Nat. Commun. 12, 4115 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Frey, S. D. Mycorrhizal fungi as mediators of soil organic matter dynamics. Annu. Rev. Ecol. Evol. Syst. 50, 237–259 (2019).

    Article  Google Scholar 

  107. Drigo, B. et al. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc. Natl Acad. Sci. USA 107, 10938–10942 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Kaiser, C. et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. N. Phytol. 205, 1537–1551 (2015).

    Article  CAS  Google Scholar 

  109. Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. N. Phytol. 209, 1705–1719 (2016).

    Article  CAS  Google Scholar 

  110. Tisserant, E. et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl Acad. Sci. USA 110, 20117–20122 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Hestrin, R., Hammer, E. C., Mueller, C. W. & Lehmann, J. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun. Biol. 2, 233 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).

    Article  CAS  PubMed  Google Scholar 

  113. Averill, C. & Hawkes, C. V. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19, 937–947 (2016).

    Article  PubMed  Google Scholar 

  114. Craig, M. E. et al. Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Glob. Change Biol. 24, 3317–3330 (2018).

    Article  Google Scholar 

  115. See, C. R. et al. Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization. Glob. Change Biol. https://doi.org/10.1111/gcb.16073 (2022).

    Article  Google Scholar 

  116. Adamczyk, B., Sietiö, O.-M., Biasi, C. & Heinonsalo, J. Interaction between tannins and fungal necromass stabilizes fungal residues in boreal forest soils. N. Phytol. 223, 16–21 (2019).

    Article  Google Scholar 

  117. Vidal, A. et al. Visualizing the transfer of organic matter from decaying plant residues to soil mineral surfaces controlled by microorganisms. Soil Biol. Biochem. 160, 108347 (2021).

    Article  CAS  Google Scholar 

  118. Kallenbach, C. M., Wallenstein, M. D., Schipanksi, M. E. & Grandy, A. S. Managing agroecosystems for soil microbial carbon use efficiency: ecological unknowns, potential outcomes, and a path forward. Front. Microbiol. 10, 1146 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Blagodatskaya, E., Blagodatsky, S., Anderson, T.-H. & Kuzyakov, Y. microbial growth and carbon use efficiency in the rhizosphere and root-free soil. PLoS ONE 9, e93282 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Domeignoz-Horta, L. A. et al. Microbial diversity drives carbon use efficiency in a model soil. Nat. Commun. 11, 3684 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Fernandez, C. W. & Kennedy, P. G. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? N. Phytol. 209, 1382–1394 (2016).

    Article  CAS  Google Scholar 

  122. Nicolas, A. M. et al. Soil candidate phyla radiation bacteria encode components of aerobic metabolism and co-occur with nanoarchaea in the rare biosphere of rhizosphere grassland communities. mSystems 6, e0120520 (2021).

    Article  PubMed  CAS  Google Scholar 

  123. Starr, E. P. et al. Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon. Microbiome 6, 122 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Pace, M. L. Bacterial mortality and the fate of bacterial production. Hydrobiologia 159, 41–49 (1988).

    Article  Google Scholar 

  125. Cram, J. A., Parada, A. E. & Fuhrman, J. A. Dilution reveals how viral lysis and grazing shape microbial communities. Limnol. Oceanogr. 61, 889–905 (2016).

    Article  Google Scholar 

  126. Ankrah, N. Y. D. et al. Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. 8, 1089–1100 (2014). This study demonstrated that in a marine environment, the mechanism of death (that is, phage infection) altered the biochemistry of microbial necromass relative to uninfected cells.

    Article  CAS  PubMed  Google Scholar 

  127. Lindeman, R. L. The trophic-dynamic aspect of ecology. Ecology 23, 399–417 (1942).

    Article  Google Scholar 

  128. Clarholm, M. Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17, 181–187 (1985).

    Article  CAS  Google Scholar 

  129. Pasternak, Z. et al. In and out: an analysis of epibiotic vs periplasmic bacterial predators. ISME J. 8, 625–635 (2014).

    Article  CAS  PubMed  Google Scholar 

  130. Lee, X., Wu, H.-J., Sigler, J., Oishi, C. & Siccama, T. Rapid and transient response of soil respiration to rain. Glob. Change Biol. 10, 1017–1026 (2004).

    Article  Google Scholar 

  131. Schimel, J. P. Life in dry soils: effects of drought on soil microbial communities and processes. Annu. Rev. Ecol. Evol. Syst. 49, 409–432 (2018).

    Article  Google Scholar 

  132. Granato, E. T., Meiller-Legrand, T. A. & Foster, K. R. The evolution and ecology of bacterial warfare. Curr. Biol. 29, R521–R537 (2019).

    Article  CAS  PubMed  Google Scholar 

  133. Bradford, M. A. et al. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Change 6, 751–758 (2016).

    Article  CAS  Google Scholar 

  134. Sierra, C. A. & Müller, M. A general mathematical framework for representing soil organic matter dynamics. Ecol. Monogr. 85, 505–524 (2015).

    Article  Google Scholar 

  135. Wang, G. et al. Microbial dormancy improves development and experimental validation of ecosystem model. ISME J. 9, 226–237 (2015).

    Article  CAS  PubMed  Google Scholar 

  136. Wieder, W., Grandy, S., Kallenbach, M. & Bonan, B. Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model. Biogeosciences 11, 3899–3917 (2014).

    Article  CAS  Google Scholar 

  137. Allison, S. D. A trait-based approach for modelling microbial litter decomposition. Ecol. Lett. 15, 1058–1070 (2012). This paper described one of the first trait-based modelling approaches to link microbial community composition with physiological and enzymatic traits to predict litter decomposition in soil.

    Article  CAS  PubMed  Google Scholar 

  138. Kaiser, C., Franklin, O., Dieckmann, U. & Richter, A. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol. Lett. 17, 680–690 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  139. Ebrahimi, A. & Or, D. Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model. Glob. Change Biol. 22, 3141–3156 (2016). This paper presented a demonstration of how to upscale results from a mechanistic model of microbial activity in soil aggregates to scales of practical interest for hydrological and climate models.

    Article  Google Scholar 

  140. Lajoie, G. & Kembel, S. W. Making the most of trait-based approaches for microbial ecology. Trends Microbiol. 27, 814–823 (2019). This opinion article discussed trait-based approaches in microbial ecology with a focus on utilization of large-scale datasets for improved ecological understanding.

    Article  CAS  PubMed  Google Scholar 

  141. Wang, G., Post, W. M. & Mayes, M. A. Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses. Ecol. Appl. 23, 255–272 (2013).

    Article  PubMed  Google Scholar 

  142. Moorhead, D. L. & Sinsabaugh, R. L. A theoretical model of litter decay and microbial interaction. Ecol. Monogr. 76, 151–174 (2006).

    Article  Google Scholar 

  143. Kooijman, S. A. L. M., Muller, E. B. & Stouthamer, A. H. Microbial growth dynamics on the basis of individual budgets. Antonie Van Leeuwenhoek 60, 159–174 (1991).

    Article  CAS  PubMed  Google Scholar 

  144. Evans, S., Dieckmann, U., Franklin, O. & Kaiser, C. Synergistic effects of diffusion and microbial physiology reproduce the Birch effect in a micro-scale model. Soil Biol. Biochem. 93, 28–37 (2016).

    Article  CAS  Google Scholar 

  145. Allison, S. D. Modeling adaptation of carbon use efficiency in microbial communities. Front. Microbiol. 5, 571 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  146. Hawkes, C. V. & Keitt, T. H. Resilience vs. historical contingency in microbial responses to environmental change. Ecol. Lett. 18, 612–625 (2015).

    Article  PubMed  Google Scholar 

  147. Tang, J. & Riley, W. J. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat. Clim. Change 5, 56–60 (2015).

    Article  CAS  Google Scholar 

  148. Zhang, Y. et al. Simulating measurable ecosystem carbon and nitrogen dynamics with the mechanistically-defined MEMS 2.0 model. Biogeosciences 18, 3147–3171 (2021).

    Article  CAS  Google Scholar 

  149. Blankinship, J. C. et al. Improving understanding of soil organic matter dynamics by triangulating theories, measurements, and models. Biogeochemistry 140, 1–13 (2018).

    Article  CAS  Google Scholar 

  150. Ebrahimi, A. N. & Or, D. Microbial dispersal in unsaturated porous media: Characteristics of motile bacterial cell motions in unsaturated angular pore networks. Water Resour. Res. 50, 7406–7429 (2014).

    Article  Google Scholar 

  151. Tang, J. & Riley, W. J. A theory of effective microbial substrate affinity parameters in variably saturated soils and an example application to aerobic soil heterotrophic respiration. J. Geophys. Res. Biogeosci. 124, 918–940 (2019).

    Article  Google Scholar 

  152. Manzoni, S., Schaeffer, S. M., Katul, G., Porporato, A. & Schimel, J. P. A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol. Biochem. 73, 69–83 (2014).

    Article  CAS  Google Scholar 

  153. Brangarí, A. C., Fernàndez-Garcia, D., Sanchez-Vila, X. & Manzoni, S. Ecological and soil hydraulic implications of microbial responses to stress – a modeling analysis. Adv. Water Resour. 116, 178–194 (2018).

    Article  Google Scholar 

  154. Alster, C. J., Weller, Z. D. & von Fischer, J. C. A meta-analysis of temperature sensitivity as a microbial trait. Glob. Change Biol. 24, 4211–4224 (2018).

    Article  Google Scholar 

  155. Wang, G., Li, W., Wang, K. & Huang, W. Uncertainty quantification of the soil moisture response functions for microbial dormancy and resuscitation. Soil Biol. Biochem. 160, 108337 (2021).

    Article  CAS  Google Scholar 

  156. Sierra, C. A., Trumbore, S. E., Davidson, E. A., Vicca, S. & Janssens, I. Sensitivity of decomposition rates of soil organic matter with respect to simultaneous changes in temperature and moisture. J. Adv. Model. Earth Syst. 7, 335–356 (2015).

    Article  Google Scholar 

  157. Nunan, N., Schmidt, H. & Raynaud, X. The ecology of heterogeneity: soil bacterial communities and C dynamics. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190249 (2020).

    Article  CAS  Google Scholar 

  158. Kaiser, C., Franklin, O., Richter, A. & Dieckmann, U. Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils. Nat. Commun. 6, 8960 (2015).

    Article  CAS  PubMed  Google Scholar 

  159. Craig, M. E., Mayes, M. A., Sulman, B. N. & Walker, A. P. Biological mechanisms may contribute to soil carbon saturation patterns. Glob. Change Biol. 27, 2633–2644 (2021).

    Article  Google Scholar 

  160. Fan, X. et al. Improved model simulation of soil carbon cycling by representing the microbially derived organic carbon pool. ISME J. 15, 2248–2263 (2021).

    Article  CAS  PubMed  Google Scholar 

  161. Sulman, B. N. et al. Multiple models and experiments underscore large uncertainty in soil carbon dynamics. Biogeochemistry 141, 109–123 (2018). This paper addressed key uncertainties in the representation of microbial degradation and mineral stabilization in five microbially explicit soil carbon models.

    Article  CAS  Google Scholar 

  162. Marschmann, G. L., Pagel, H., Kügler, P. & Streck, T. Equifinality, sloppiness, and emergent structures of mechanistic soil biogeochemical models. Environ. Model. Softw. 122, 104518 (2019).

    Article  Google Scholar 

  163. Martiny, J. B. H., Jones, S. E., Lennon, J. T. & Martiny, A. C. Microbiomes in light of traits: a phylogenetic perspective. Science 350, aac9323 (2015).

    Article  PubMed  CAS  Google Scholar 

  164. Malik, A. A., Thomson, B. C., Whiteley, A. S., Bailey, M. & Griffiths, R. I. Bacterial physiological adaptations to contrasting edaphic conditions identified using landscape scale metagenomics. mBio 8, e00799-17 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  165. Westoby, M. et al. Trait dimensions in bacteria and archaea compared to vascular plants. Ecol. Lett. 24, 1487–1504 (2021).

    Article  PubMed  Google Scholar 

  166. Jung, M.-Y. et al. Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. ISME J. 16, 272–283 (2022).

    Article  CAS  PubMed  Google Scholar 

  167. Kempes, C. P., Wang, L., Amend, J. P., Doyle, J. & Hoehler, T. Evolutionary tradeoffs in cellular composition across diverse bacteria. ISME J. 10, 2145–2157 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Dethlefsen, L. & Schmidt, T. M. Performance of the translational apparatus varies with the ecological strategies of bacteria. J. Bacteriol. 189, 3237–3245 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Andersen, K. H. et al. Characteristic sizes of life in the oceans, from bacteria to whales. Annu. Rev. Mar. Sci. 8, 217–241 (2016).

    Article  CAS  Google Scholar 

  170. Malik, A. A. et al. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J. 14, 1–9 (2020).

    Article  CAS  PubMed  Google Scholar 

  171. Weissman, J. L., Hou, S. & Fuhrman, J. A. Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns. Proc. Natl Acad. Sci. USA 118, e2016810118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Li, G., Rabe, K. S., Nielsen, J. & Engqvist, M. K. M. Machine learning applied to predicting microorganism growth temperatures and enzyme catalytic optima. ACS Synth. Biol. 8, 1411–1420 (2019).

    Article  CAS  PubMed  Google Scholar 

  173. Hungate, B. A. et al. Quantitative microbial ecology through stable isotope probing. Appl. Environ. Microbiol. 81, 7570–7581 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Couradeau, E. et al. Probing the active fraction of soil microbiomes using BONCAT-FACS. Nat. Commun. 10, 2770 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  175. Starr, E. P. et al. Stable-isotope-informed, genome-resolved metagenomics uncovers potential cross-kingdom interactions in rhizosphere soil. mSphere 6, e0008521 (2021).

    Article  PubMed  Google Scholar 

  176. Rousk, J. & Bååth, E. Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol. Ecol. 62, 258–267 (2007).

    Article  CAS  PubMed  Google Scholar 

  177. Koechli, C., Campbell, A. N., Pepe-Ranney, C. & Buckley, D. H. Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing. Soil Biol. Biochem. 130, 150–158 (2019).

    Article  CAS  Google Scholar 

  178. Wilhelm, R. C., Singh, R., Eltis, L. D. & Mohn, W. W. Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. ISME J. 13, 413–429 (2019).

    Article  CAS  PubMed  Google Scholar 

  179. Neurath, R. A. et al. Root carbon interaction with soil minerals is dynamic, leaving a legacy of microbially derived residues. Environ. Sci. Technol. 55, 13345–13355 (2021).

    CAS  PubMed  Google Scholar 

  180. Luo, Y. et al. Rice rhizodeposition promotes the build-up of organic carbon in soil via fungal necromass. Soil Biol. Biochem. 160, 108345 (2021).

    Article  CAS  Google Scholar 

  181. Carini, P. et al. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat. Microbiol. 2, 16242 (2016).

    Article  PubMed  CAS  Google Scholar 

  182. Sharma, K., Palatinszky, M., Nikolov, G., Berry, D. & Shank, E. A. Transparent soil microcosms for live-cell imaging and non-destructive stable isotope probing of soil microorganisms. eLife 9, e56275 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Arellano-Caicedo, C., Ohlsson, P., Bengtsson, M., Beech, J. P. & Hammer, E. C. Habitat geometry in artificial microstructure affects bacterial and fungal growth, interactions, and substrate degradation. Commun. Biol. 4, 1226 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  184. Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).

    Article  CAS  PubMed  Google Scholar 

  185. García-Palacios, P. et al. Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. Nat. Rev. Earth Env. 2, 507–517 (2021).

    Article  Google Scholar 

  186. Schulz, F. et al. Hidden diversity of soil giant viruses. Nat. Commun. 9, 4881 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  187. Trubl, G. et al. Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ 7, e7265 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  188. Guo, J. et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 9, 37 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  189. Sommers, P., Chatterjee, A., Varsani, A. & Trubl, G. Integrating viral metagenomics into an ecological framework. Annu. Rev. Virol. 8, 133–158 (2021).

    Article  PubMed  CAS  Google Scholar 

  190. Pratama, A. A. & van Elsas, J. D. The ‘neglected’ soil virome–potential role and impact. Trends Microbiol. 26, 649–662 (2018).

    Article  CAS  PubMed  Google Scholar 

  191. Ghosh, D. et al. Prevalence of lysogeny among soil bacteria and presence of 16S rRNA and trzN genes in viral-community DNA. Appl. Environ. Microbiol. 74, 495–502 (2008).

    Article  CAS  PubMed  Google Scholar 

  192. Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).

    Article  CAS  PubMed  Google Scholar 

  193. Howard-Varona, C. et al. Phage-specific metabolic reprogramming of virocells. ISME J. 14, 881–895 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  194. Howard-Varona, C. et al. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME J. 12, 1605–1618 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Van Goethem, M. Characteristics of wetting-induced bacteriophage blooms in biological soil crust. mBio 10, e02287-19 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  196. Trubl, G. et al. Active virus-host interactions at sub-freezing temperatures in Arctic peat soil. Microbiome 9, 208 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Lee, S. et al. Methane-derived carbon flows into host–virus networks at different trophic levels in soil. Proc. Natl Acad. Sci. USA 118, e2105124118 (2021). This study used stable isotope probing metagenomics to connect, in situ, active virus–host infections with the biogeochemical process of methane oxidation in soil.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B. L. & Sullivan, M. B. iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure. ISME J. 11, 7–14 (2017).

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank the Lawrence Livermore National Laboratory (LLNL) Soil Microbiome Scientific Focus Area team for helpful discussions, and K. Georgiou and E. Whalen for providing comments on earlier drafts of the manuscript. This work was supported by the U.S. Department of Energy (DOE), Office of Biological and Environmental Research, Genomic Science Program (GSP) LLNL ‘Microbes Persist’ Soil Microbiome Scientific Focus Area SCW1632. Work at LLNL was performed under the auspices of the DOE, Contract DE-AC52-07NA27344. Part of this work was performed at Lawrence Berkeley National Laboratory funded under U.S. Department of Energy contract number DE-AC02-05CH11231.

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Authors and Affiliations

  1. Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA

    Noah W. Sokol, Eric Slessarev, Steven J. Blazewicz, Rachel Hestrin, Gareth Trubl, Karis McFarlane, Rhona Stuart, Erin Nuccio, Peter Weber, Yongqin Jiao, Mavrik Zavarin, Jeffrey Kimbrel, Keith Morrison, Dinesh Adhikari, Amrita Bhattacharaya & Jennifer Pett-Ridge

  2. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Gianna L. Marschmann, Eoin L. Brodie, Amrita Bhattacharaya, Peter Nico, Jinyun Tang & Jillian Banfield

  3. Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA

    Alexa Nicolas

  4. Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, CA, USA

    Eoin L. Brodie, Mary K. Firestone, Alex Greenlon, Ella T. Sieradzki, Rohan Sachdeva & Jillian Banfield

  5. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA

    Megan M. Foley, Bruce A. Hungate, Benjamin J. Koch & Paul Dijkstra

  6. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA

    Megan M. Foley, Bruce A. Hungate, Benjamin J. Koch, Paul Dijkstra & Egbert Schwartz

  7. Earth and Biological Science Directorate, Pacific Northwest National Laboratory, Richland, WA, USA

    Bram W. Stone

  8. Department of Microbiology, Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan & Olivier Zablocki

  9. Center of Microbiome Science, Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan & Olivier Zablocki

  10. Department of Civil, Environmental and Geodetic Engineering, Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan

  11. Life and Environmental Sciences Department, University of California Merced, Merced, CA, USA

    Jennifer Pett-Ridge

  12. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, USA

    Nicole Didonato & Ljiljana Paša-Tolić

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  1. Noah W. Sokol
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Consortia

LLNL Soil Microbiome Consortium

  • Noah W. Sokol
  • , Eric Slessarev
  • , Gianna L. Marschmann
  • , Alexa Nicolas
  • , Steven J. Blazewicz
  • , Eoin L. Brodie
  • , Mary K. Firestone
  • , Megan M. Foley
  • , Rachel Hestrin
  • , Bruce A. Hungate
  • , Benjamin J. Koch
  • , Bram W. Stone
  • , Matthew B. Sullivan
  • , Olivier Zablocki
  • , Jennifer Pett-Ridge
  • , Gareth Trubl
  • , Karis McFarlane
  • , Rhona Stuart
  • , Erin Nuccio
  • , Peter Weber
  • , Yongqin Jiao
  • , Mavrik Zavarin
  • , Jeffrey Kimbrel
  • , Keith Morrison
  • , Dinesh Adhikari
  • , Amrita Bhattacharaya
  • , Peter Nico
  • , Jinyun Tang
  • , Nicole Didonato
  • , Ljiljana Paša-Tolić
  • , Alex Greenlon
  • , Ella T. Sieradzki
  • , Paul Dijkstra
  • , Egbert Schwartz
  • , Rohan Sachdeva
  •  & Jillian Banfield

Contributions

N.W.S., E.S., G.L.M., A.N., S.J.B., E.L.B., M.M.F., R.H., B.A.H., B.J.K., B.W.S., O.Z. and J.P.-R. wrote the article. All main authors helped contribute to discussions of the content and reviewed or edited the article before submission. The Consortium contributed to several ideas in the manuscript, particularly to Table 1.

Corresponding authors

Correspondence to Noah W. Sokol or Jennifer Pett-Ridge.

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Related links

microTrait: https://github.com/ukaraoz/microtrait

Glossary

Microbial necromass

Dead cellular biomass (for example, cell envelopes) and extracellular products (for example, extracellular polymeric substances).

Ecological succession

A consistent, distinct trajectory of community change through time.

Rhizosphere

The zone of soil under direct influence of a living plant root.

Hyphosphere

The zone of soil under direct influence of fungal hyphae.

Detritusphere

The zone of soil under direct influence of decaying litter.

Bulk soil

Soil that is not in the direct influence of living or dead roots; characterized by lower levels of microbial density and activity relative to high-resource habitats.

Ecophysiological traits

Traits related to the physiology of a microorganism, as shaped by their biotic and abiotic ecological context.

Mineral-associated organic matter

Soil organic matter that exists in some degree of association with soil minerals.

Carbon-use efficiency

(CUE). Microbial biomass yield given a quantity of available substrate.

Community assembly

Processes that shape the identity and abundance of species within a biological community.

Mutualism

A form of symbiosis where both partners benefit.

Density-dependent

A process that regulates population size based on population density.

Viral shunt

The theory that viral lysis of microbial cells returns labile organic matter to an available pool.

Exploitative competition

Indirect competition for resources.

Antagonistic competition

Direct competition involving combative interactions.

Trophic transfer

The transfer of energy between trophic levels.

Microbial loop

The flux of nutrients, energy and organic matter within microbial communities.

Birch effect

The ephemeral pulse of CO2 following wetting of dry soil.

Microbially explicit biogeochemical models

Models that represent the amount of microbial biomass as a dynamic variable that mediates biogeochemical transformation rates.

Trait inference

Indirect trait quantification based on genomic data, as opposed to direct observation of microbial trait.

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Sokol, N.W., Slessarev, E., Marschmann, G.L. et al. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat Rev Microbiol 20, 415–430 (2022). https://doi.org/10.1038/s41579-022-00695-z

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