Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Formation of necromass-derived soil organic carbon determined by microbial death pathways

Abstract

Soil organic matter is the dominant carbon pool in terrestrial ecosystems, and its management is of increasing policy relevance. Soil microbes are the main drivers of soil organic carbon sequestration, especially through accumulation of their necromass. However, since the direct characterization of microbial necromass in soil is challenging, its composition and formation remain unresolved. Here we provide evidence that microbial death pathways (the distinct processes of microbial dying) in soil affect necromass composition and its subsequent fate. Importantly, the composition of derived microbial necromass does not equal that of microbial biomass. From biomass to necromass, distinct chemical transformations lead to increases in cell wall/cytoplasm ratios while nutrient contents and easily degradable compounds are depleted. The exact changes depend on environmental conditions and the relevance of different microbial death pathways, for example, predation, starvation or anthropogenic stresses. This has far-reaching consequences for mechanisms underpinning biogeochemical processes: (1) the quantity and persistence of microbial necromass is governed by microbial death pathways, not only the initial biomass composition; (2) efficient recycling of nutrients within microbial biomass presents a possible pathway of organic carbon sequestration that minimizes nitrogen losses; (3) human-induced disturbances affect the causes of microbial death and consequently necromass composition. Thus, new research focusing on microbial death pathways holds great potential to improve management strategies for soil organic carbon storage. Not only microbial growth but also death drive the soil microbial carbon pump.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Visual illustration of MDPs, including molecular transformations from microbial biomass to necromass.
Fig. 2: Visualizing the dependencies of MDPs on biotic and abiotic soil properties and environmental factors.

Similar content being viewed by others

References

  1. Bradford, M. A. et al. Soil carbon science for policy and practice. Nat. Sustain. 2, 1070–1072 (2019).

    Article  Google Scholar 

  2. Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).

    Article  Google Scholar 

  3. 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  Google Scholar 

  4. 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).

    Article  Google Scholar 

  5. Wang, B. R., An, S. S., Liang, C., Liu, Y. & Kuzyakov, Y. Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biol. Biochem. 162, 108422 (2021).

    Article  Google Scholar 

  6. Kästner, M. & Miltner, A. in The Future of Soil Carbon (eds Garcia, C. et al.) Ch. 5 (Academic Press, 2018).

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

    Article  Google Scholar 

  8. 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  Google Scholar 

  9. 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).

    Article  Google Scholar 

  10. Emerson, J. B. et al. Schrödinger’s microbes: tools for distinguishing the living from the dead in microbial ecosystems. Microbiome 5, 86 (2017).

    Article  Google Scholar 

  11. 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  Google Scholar 

  12. Ackermann, M., Stearns Stephen, C. & Jenal, U. Senescence in a bacterium with asymmetric division. Science 300, 1920–1920 (2003).

    Article  Google Scholar 

  13. Aguilaniu, H., Gustafsson, L., Rigoulet, M. & Nyström, T. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299, 1751–1753 (2003).

    Article  Google Scholar 

  14. Maheshwari, R. & Navaraj, A. Senescence in fungi: the view from Neurospora. FEMS Microbiol. Lett. 280, 135–143 (2008).

    Article  Google Scholar 

  15. 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. 28, 2527–2540 (2022).

    Article  Google Scholar 

  16. Pusztahelyi, T. et al. Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia Microbiologica 51, 547–554 (2006).

    Article  Google Scholar 

  17. Bartoszewska, M. & Kiel, J. A. The role of macroautophagy in development of filamentous fungi. Antioxid. Redox Signal. 14, 2271–2287 (2011).

    Article  Google Scholar 

  18. Josefsen, L. et al. Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum. Autophagy 8, 326–337 (2012).

    Article  Google Scholar 

  19. Heaton, L. L., Jones, N. S. & Fricker, M. D. Energetic constraints on fungal growth. Am. Nat. 187, E27–E40 (2016).

    Article  Google Scholar 

  20. Taiz, L. & Zeiger, E. Plant Physiology 4th edn (Spektrum Akademischer Verlag, 2008).

  21. Bowman, E. J. & Bowman, B. J. in Cellular and Molecular Biology of Filamentous Fungi (eds Borkovich, K. & Ebbole, D.) 179–190 (ASM Press, 2010).

  22. Voigt, O. & Pöggeler, S. Self-eating to grow and kill: autophagy in filamentous ascomycetes. Appl. Microbiol. Biotechnol. 97, 9277–9290 (2013).

    Article  Google Scholar 

  23. Grimmett, I. J., Shipp, K. N., Macneil, A. & Barlocher, F. Does the growth rate hypothesis apply to aquatic hyphomycetes? Fungal Ecol. 6, 493–500 (2013).

    Article  Google Scholar 

  24. Camenzind, T., Philipp Grenz, K., Lehmann, J. & Rillig, M. C. Soil fungal mycelia have unexpectedly flexible stoichiometric C:N and C:P ratios. Ecol. Lett. 24, 208–218 (2021).

    Article  Google Scholar 

  25. Mason-Jones, K., Robinson, S. L., Veen, G. F., Manzoni, S. & van der Putten, W. H. Microbial storage and its implications for soil ecology. ISME J. 16, 617–629 (2022).

    Article  Google Scholar 

  26. Gow, N. A. R., Latge, J. P. & Munro, C. A. The fungal cell wall: structure, biosynthesis, and function. Microbiol. Spectr. 5, FUNK-0035–2016 (2017).

    Article  Google Scholar 

  27. Steiner, U. K. Senescence in bacteria and its underlying mechanisms. Front. Cell Dev. Biol. 9, 668915 (2021).

    Article  Google Scholar 

  28. Allocati, N., Masulli, M., Di Ilio, C. & De Laurenzi, V. Die for the community: an overview of programmed cell death in bacteria. Cell Death Dis. 6, e1609 (2015).

    Article  Google Scholar 

  29. Peeters, S. H. & de Jonge, M. I. For the greater good: programmed cell death in bacterial communities. Microbiol. Res. 207, 161–169 (2018).

    Article  Google Scholar 

  30. Wang, J. & Bayles, K. W. Programmed cell death in plants: lessons from bacteria? Trends Plant Sci. 18, 133–139 (2013).

    Article  Google Scholar 

  31. Nagamalleswari, E., Rao, S., Vasu, K. & Nagaraja, V. Restriction endonuclease triggered bacterial apoptosis as a mechanism for long time survival. Nucleic Acids Res. 45, 8423–8434 (2017).

    Article  Google Scholar 

  32. Kysela, D. T., Brown, P. J. B., Huang, K. C. & Brun, Y. V. Biological consequences and advantages of asymmetric bacterial growth. Annu. Rev. Microbiol. 67, 417–435 (2013).

    Article  Google Scholar 

  33. Bayles, K. W. Bacterial programmed cell death: making sense of a paradox. Nat. Rev. Microbiol. 12, 63–69 (2014).

    Article  Google Scholar 

  34. Flemming, H.-C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).

    Article  Google Scholar 

  35. Coleman, D. C. & Wall, D. H. in Soil Microbiology, Ecology and Biochemistry 4th edn (ed. Paul, E. A.) Ch. 5 (Academic Press, 2015).

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

    Article  Google Scholar 

  37. Kuzyakov, Y. & Mason-Jones, K. Viruses in soil: nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions. Soil Biol. Biochem. 127, 305–317 (2018).

    Article  Google Scholar 

  38. 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).

    Article  Google Scholar 

  39. Sokol, N. W. et al. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat. Rev. Microbiol. 20, 415–430 (2022).

    Article  Google Scholar 

  40. Bonkowski, M. & Clarholm, M. J. A. P. Stimulation of plant growth through interactions of bacteria and protozoa: testing the auxiliary microbial loop hypothesis. Acta Protozool. 51, 237–247 (2012).

    Google Scholar 

  41. Potapov, A. M., Pollierer, M. M., Salmon, S., Šustr, V. & Chen, T.-W. Multidimensional trophic niche revealed by complementary approaches: gut content, digestive enzymes, fatty acids and stable isotopes in Collembola. J. Anim. Ecol. 90, 1919–1933 (2021).

    Article  Google Scholar 

  42. Esteban, G. F. & Fenchel, T. M. in Ecology of Protozoa: The Biology of Free-living Phagotrophic Protists (eds Esteban, G. F. & Fenchel, T. M.) 33–54 (Springer, 2020).

  43. Koksharova, O. A. Bacteria and phenoptosis. Biochemistry 78, 963–970 (2013).

    Google Scholar 

  44. Tilman, D. Resource Competition and Community Structure (Princeton Univ. Press, 1982).

  45. Boddy, L. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol. 31, 185–194 (2000).

    Article  Google Scholar 

  46. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).

    Article  Google Scholar 

  47. Müller, S. et al. Predation by Myxococcus xanthus induces Bacillus subtilis to form spore-filled megastructures. Appl. Environ. Microbiol. 81, 203–210 (2015).

    Article  Google Scholar 

  48. Laskowska, E. & Kuczynska-Wisnik, D. New insight into the mechanisms protecting bacteria during desiccation. Curr. Genet. 66, 313–318 (2020).

    Article  Google Scholar 

  49. Rillig, M. C., Ryo, M. & Lehmann, A. Classifying human influences on terrestrial ecosystems. Glob. Change Biol. 27, 2273–2278 (2021).

    Article  Google Scholar 

  50. Dörr, T., Moynihan, P. J. & Mayer, C. Bacterial cell wall structure and dynamics. Front. Microbiol. 10, 02051 (2019).

    Article  Google Scholar 

  51. Corredor, B., Lang, B. & Russell, D. Effects of nitrogen fertilization on soil fauna in a global meta-analysis. Preprint at Res. Sq. https://doi.org/10.21203/rs.3.rs-1438491/v1 (2022).

  52. Blankinship, J. C., Niklaus, P. A. & Hungate, B. A. A meta-analysis of responses of soil biota to global change. Oecologia 165, 553–565 (2011).

    Article  Google Scholar 

  53. Manzoni, S., Chakrawal, A., Spohn, M. & Lindahl, B. D. Modeling microbial adaptations to nutrient limitation during litter decomposition. Front. For. Glob. Change 4, 686945 (2021).

    Article  Google Scholar 

  54. Frank, D. et al. Effects of climate extremes on the terrestrial carbon cycle: concepts, processes and potential future impacts. Glob. Change Biol. 21, 2861–2880 (2015).

    Article  Google Scholar 

  55. Gunina, A. & Kuzyakov, Y. From energy to (soil organic) matter. Glob. Change Biol. 28, 2169–2182 (2022).

    Article  Google Scholar 

  56. Fernandez, C. W. & Koide, R. T. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol. Biochem. 77, 150–157 (2014).

    Article  Google Scholar 

  57. Kästner, M., Miltner, A., Thiele-Bruhn, S. & Liang, C. Microbial necromass in soils—linking microbes to soil processes and carbon turnover. Front. Environ. Sci. 9, 756378 (2021).

    Article  Google Scholar 

  58. Buckeridge, K. M., Creamer, C. & Whitaker, J. Deconstructing the microbial necromass continuum to inform soil carbon sequestration. Funct. Ecol. 36, 1396–1410 (2022).

    Article  Google Scholar 

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

    Article  Google Scholar 

  60. 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).

    Article  Google Scholar 

  61. 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  Google Scholar 

  62. Liang, C. Soil microbial carbon pump: mechanism and appraisal. Soil Ecol. Lett. 2, 241–254 (2020).

    Article  Google Scholar 

  63. Sinsabaugh, R. L., Manzoni, S., Moorhead, D. L. & Richter, A. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol. Lett. 16, 930–939 (2013).

    Article  Google Scholar 

  64. van Groenigen, J. W. et al. Sequestering soil organic carbon: a nitrogen dilemma. Environ. Sci. Technol. 51, 4738–4739 (2017).

    Article  Google Scholar 

  65. Greenlon, A. et al. Quantitative stable-isotope probing (qSIP) with metagenomics links microbial physiology and activity to soil moisture in Mediterranean-climate grassland ecosystems (in the press).

  66. Mafla-Endara, P. M. et al. Microfluidic chips provide visual access to in situ soil ecology. Commun. Biol. 4, 889 (2021).

    Article  Google Scholar 

  67. Schaible, G. A., Kohtz, A. J., Cliff, J. & Hatzenpichler, R. Correlative SIP-FISH-Raman-SEM-NanoSIMS links identity, morphology, biochemistry, and physiology of environmental microbes. ISME Commun. 2, 52 (2022).

    Article  Google Scholar 

  68. See, C. R. et al. Distinct carbon fractions drive a generalisable two-pool model of fungal necromass decomposition. Funct. Ecol. 35, 796–806 (2021).

    Article  Google Scholar 

  69. Wang, C. et al. Stabilization of microbial residues in soil organic matter after two years of decomposition. Soil Biol. Biochem. 141, 107687 (2020).

    Article  Google Scholar 

  70. Veresoglou, S. D., Halley, J. M. & Rillig, M. C. Extinction risk of soil biota. Nat. Commun. 6, 8862 (2015).

    Article  Google Scholar 

  71. Potapov, A. M. et al. Feeding habits and multifunctional classification of soil-associated consumers from protists to vertebrates. Biol. Rev. 97, 1057–1117 (2022).

    Article  Google Scholar 

  72. Trap, J., Bonkowski, M., Plassard, C., Villenave, C. & Blanchart, E. Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398, 1–24 (2016).

    Article  Google Scholar 

  73. Dooley, S. R. & Treseder, K. K. The effect of fire on microbial biomass: a meta-analysis of field studies. Biogeochemistry 109, 49–61 (2012).

    Article  Google Scholar 

  74. Muñoz-Leoz, B., Ruiz-Romera, E., Antigüedad, I. & Garbisu, C. Tebuconazole application decreases soil microbial biomass and activity. Soil Biol. Biochem. 43, 2176–2183 (2011).

    Article  Google Scholar 

  75. Meyer, M., Diehl, D., Schaumann, G. E. & Muñoz, K. Agricultural mulching and fungicides—impacts on fungal biomass, mycotoxin occurrence, and soil organic matter decomposition. Environ. Sci. Pollut. Res. 28, 36535–36550 (2021).

    Article  Google Scholar 

  76. Thiery, S. & Kaimer, C. The predation strategy of Myxococcus xanthus. Front. Microbiol. 11, 2 (2020).

    Article  Google Scholar 

  77. Laloux, G. Shedding light on the cell biology of the predatory bacterium Bdellovibrio bacteriovorus. Front. Microbiol. 10, 3136 (2020).

    Article  Google Scholar 

Download references

Acknowledgements

T.C. acknowledges funding by the Deutsche Forschungsgemeinschaft (grant number 465123751, SPP2322 SoilSystems). K.M.-J. acknowledges the Dutch Research Council (NWO) for funding of the Veni project VI.Veni.202.086. We thank S. Maaß and M. Maraun for valuable input on the feeding habits of fauna in soil.

Author information

Authors and Affiliations

Authors

Contributions

T.C. and J.L. generated the initial conceptual ideas. T.C. led the writing and literature search. K.M.-J., I.M., M.C.R., J.L. and T.C. developed the final concepts. All authors contributed to writing and editing.

Corresponding author

Correspondence to Tessa Camenzind.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Geoscience thanks Joshua Schimel, Cynthia Kallenbach and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Xujia Jiang, in collaboration with the Nature Geoscience team.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Camenzind, T., Mason-Jones, K., Mansour, I. et al. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat. Geosci. 16, 115–122 (2023). https://doi.org/10.1038/s41561-022-01100-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-022-01100-3

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing