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:

Redox control on rhizosphere priming in wetlands

Abstract

Rhizosphere priming describes a positive or negative change in the rate of soil organic matter decomposition caused by root activity and represents an important terrestrial soil–climate feedback. Few studies have investigated rhizosphere priming in wetlands, despite their disproportionate role in the global soil carbon budget. Here we present a literature analysis to show that both positive and negative rhizosphere priming can be much stronger in wetland than upland ecosystems. We argue that differences in plant–soil microbial interactions between dominantly oxic and anoxic soil environments induce the different degrees of rhizosphere priming effects. A conceptual framework is proposed in which wetland plants control soil redox status by acting as sources of both electron donors and acceptors, thereby influencing soil carbon stability through interactions with microbial communities. We identify key uncertainties in the mechanistic and quantitative understanding of wetland rhizosphere priming and demonstrate how priming could govern wetland soil carbon dynamics and ecosystem stability in response to climate change.

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: Distribution of rhizosphere priming effects.
Fig. 2: Comparison of rhizosphere priming effects.
Fig. 3: Redox mediation of wetland rhizosphere priming.

Similar content being viewed by others

Data availability

Data are available from our OSF data repository at https://doi.org/10.17605/OSF.IO/4V73N.

References

  1. Bardgett, R. D., Freeman, C. & Ostle, N. J. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2, 805–814 (2008).

    CAS  Google Scholar 

  2. Keuper, F. et al. Carbon loss from northern circumpolar permafrost soils amplified by rhizosphere priming. Nat. Geosci. 13, 560–565 (2020).

    CAS  Google Scholar 

  3. Hartley, I. P. et al. A potential loss of carbon associated with greater plant growth in the European Arctic. Nat. Clim. Chang. 2, 875–879 (2012).

    CAS  Google Scholar 

  4. Kuzyakov, Y. Review: factors affecting rhizosphere priming effects. J. Plant Nutr. Soil Sci. 165, 382–396 (2002).

    CAS  Google Scholar 

  5. Huo, C., Luo, Y. & Cheng, W. Rhizosphere priming effect: a meta-analysis. Soil Biol. Biochem. 111, 78–84 (2017).

    CAS  Google Scholar 

  6. Dijkstra, F. A., Zhu, B. & Cheng, W. Root effects on soil organic carbon: a double-edged sword. N. Phytol. 230, 60–65 (2021).

    CAS  Google Scholar 

  7. Gorham, E. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol. Appl. 1, 182–195 (1991).

    Google Scholar 

  8. Temmink, R. J. M. et al. Recovering wetland biogeomorphic feedbacks to restore the world’s biotic carbon hotspots. Science 376, 6593 (2022).

    Google Scholar 

  9. Armstrong, W. Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol. Plant. 25, 192–197 (1971).

    Google Scholar 

  10. Wolf, A. A., Drake, B. G., Erickson, J. E. & Megonigal, J. P. An oxygen-mediated positive feedback between elevated carbon dioxide and soil organic matter decomposition in a simulated anaerobic wetland. Glob. Chang. Biol. 13, 2036–2044 (2007).

    Google Scholar 

  11. Keiluweit, M., Nico, P. S., Kleber, M. & Fendorf, S. Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils? Biogeochemistry 127, 157–171 (2016).

    CAS  Google Scholar 

  12. Blagodatskaya, Е. & Kuzyakov, Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol. Fertil. Soils 45, 115–131 (2008).

    Google Scholar 

  13. Zwetsloot, M. J., Kessler, A. & Bauerle, T. L. Phenolic root exudate and tissue compounds vary widely among temperate forest tree species and have contrasting effects on soil microbial respiration. N. Phytol. 218, 530–541 (2018).

    CAS  Google Scholar 

  14. Keiluweit, M. et al. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Chang. 5, 588–595 (2015).

    CAS  Google Scholar 

  15. Wang, X., Tang, C., Severi, J., Butterly, C. R. & Baldock, J. A. Rhizosphere priming effect on soil organic carbon decomposition under plant species differing in soil acidification and root exudation. N. Phytol. 211, 864–873 (2016).

    CAS  Google Scholar 

  16. Lu, J., Dijkstra, F. A., Wang, P. & Cheng, W. Roots of non-woody perennials accelerated long-term soil organic matter decomposition through biological and physical mechanisms. Soil Biol. Biochem. 134, 42–53 (2019).

    CAS  Google Scholar 

  17. Hodge, A., Stewart, J., Robinson, D., Griffiths, B. S. & Fitter, A. H. Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J. Ecol. 88, 150–164 (2000).

    Google Scholar 

  18. Burgin, A. J. & Loecke, T. D. The biogeochemical redox paradox: how can we make a foundational concept more predictive of biogeochemical state changes? Biogeochemistry 164, 349–370 (2023).

    Google Scholar 

  19. Dijkstra, F. A., Carrillo, Y., Pendall, E. & Morgan, J. A. Rhizosphere priming: a nutrient perspective. Front. Microbiol. 4, 216 (2013).

    CAS  Google Scholar 

  20. Neubauer, S. C. & Megonigal, J. P. in Wetland Carbon and Environmental Management (eds Krauss, K. W. et al.) Ch. 3 (American Geophysical Union, 2021); https://doi.org/10.1002/9781119639305.ch3

  21. Zhu, E. et al. Organic carbon and lignin protection by metal oxides versus silicate clay: comparative study based on wetland and upland soils. J. Geophys. Res. Biogeosci. 128, e2023JG007474 (2023).

    CAS  Google Scholar 

  22. Wang, Y., Wang, H., He, J. S. & Feng, X. Iron-mediated soil carbon response to water-table decline in an alpine wetland. Nat. Commun. 8, 15972 (2017).

    CAS  Google Scholar 

  23. Freeman, C., Ostle, N. & Kang, H. An enzymic ‘latch’ on a global carbon store. Nature 409, 149–150 (2001).

    CAS  Google Scholar 

  24. Hall, S. J., Treffkorn, J. & Silver, W. L. Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils. Ecology 95, 2964–2973 (2014).

    Google Scholar 

  25. Agethen, S. & Knorr, K. H. Juncus effusus mono-stands in restored cutover peat bogs – analysis of litter quality, controls of anaerobic decomposition, and the risk of secondary carbon loss. Soil Biol. Biochem. 117, 139–152 (2018).

    CAS  Google Scholar 

  26. Wild, B., Monteux, S., Wendler, B., Hugelius, G. & Keuper, F. Circum-Arctic peat soils resist priming by plant-derived compounds. Soil Biol. Biochem. 180, 109012 (2023).

    CAS  Google Scholar 

  27. Cui, J. et al. Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biol. Biochem. 142, 107720 (2020).

    CAS  Google Scholar 

  28. Liu, L. et al. Carbon stock stability in drained peatland after simulated plant carbon addition: strong dependence on deeper soil. Sci. Total Environ. 848, 157539 (2022).

    CAS  Google Scholar 

  29. Deroo, H. et al. Effect of organic carbon addition on paddy soil organic carbon decomposition under different irrigation regimes. Biogeosciences 18, 5035–5051 (2021).

    CAS  Google Scholar 

  30. Zhang, Q. et al. A distinct sensitivity to the priming effect between labile and stable soil organic carbon. N. Phytol. 237, 88–99 (2023).

    CAS  Google Scholar 

  31. Kramer, M. G. & Chadwick, O. A. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat. Clim. Chang. 8, 1104–1108 (2018).

    CAS  Google Scholar 

  32. Grybos, M., Davranche, M., Gruau, G., Petitjean, P. & Pédrot, M. Increasing pH drives organic matter solubilization from wetland soils under reducing conditions. Geoderma 154, 13–19 (2009).

    CAS  Google Scholar 

  33. Afsar, M. Z., Vasilas, B. & Jin, Y. Organo-mineral associations and size-fractionated colloidal organic carbon dynamics in a redox-controlled wetland. Geoderma 439, 116667 (2023).

    CAS  Google Scholar 

  34. Bai, J. et al. Iron-bound carbon increases along a freshwater-oligohaline gradient in a subtropical tidal wetland. Soil Biol. Biochem. 154, 108128 (2021).

    CAS  Google Scholar 

  35. Lin, Y. et al. Differential effects of redox conditions on the decomposition of litter and soil organic matter. Biogeochemistry 154, 1–15 (2021).

    CAS  Google Scholar 

  36. Boye, K. et al. Thermodynamically controlled preservation of organic carbon in floodplains. Nat. Geosci. 10, 415–419 (2017).

    CAS  Google Scholar 

  37. Canarini, A., Kaiser, C., Merchant, A., Richter, A. & Wanek, W. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10, 157 (2019).

    Google Scholar 

  38. Sogin, E. M. et al. Sugars dominate the seagrass rhizosphere. Nat. Ecol. Evol. 6, 866–877 (2022).

    Google Scholar 

  39. Mueller, P. et al. Plant species determine tidal wetland methane response to sea level rise. Nat. Commun. 11, 5154 (2020).

    CAS  Google Scholar 

  40. Agethen, S., Sander, M., Waldemer, C. & Knorr, K. H. Plant rhizosphere oxidation reduces methane production and emission in rewetted peatlands. Soil Biol. Biochem. 125, 125–135 (2018).

    CAS  Google Scholar 

  41. Bradley, P. M. & Morris, J. T. Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71, 282–287 (1990).

    CAS  Google Scholar 

  42. Koop-Jakobsen, K., Mueller, P., Meier, R. J., Liebsch, G. & Jensen, K. Plant-sediment interactions in salt marshes – an optode imaging study of O2, pH and CO2 gradients in the rhizosphere. Front. Plant Sci. 9, 541 (2018).

    Google Scholar 

  43. Zhong, Z. et al. The root tip of submerged plants: an efficient engine for carbon mineralization. Environ. Sci. Technol. Lett. 10, 385–390 (2023).

    CAS  Google Scholar 

  44. Mueller, P., Jensen, K. & Megonigal, J. P. Plants mediate soil organic matter decomposition in response to sea level rise. Glob. Chang. Biol. 22, 404–414 (2016).

    Google Scholar 

  45. Naughton, H. R. et al. Development of energetic and enzymatic limitations on microbial carbon cycling in soils. Biogeochemistry 153, 191–213 (2021).

    CAS  Google Scholar 

  46. McGivern, B. B. et al. Decrypting bacterial polyphenol metabolism in an anoxic wetland soil. Nat. Commun. 12, 2466 (2021).

    CAS  Google Scholar 

  47. Ayi, Q. et al. Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants. Ann. Bot. 118, 674–683 (2016).

    Google Scholar 

  48. Maricle, B. R. & Lee, R. W. Root respiration and oxygen flux in salt marsh grasses from different elevational zones. Mar. Biol. 151, 413–423 (2007).

    Google Scholar 

  49. Yu, C., Xie, S., Song, Z., Xia, S. & Åström, M. E. Biogeochemical cycling of iron (hydr-)oxides and its impact on organic carbon turnover in coastal wetlands: a global synthesis and perspective. Earth Sci. Rev. 218, 103658 (2021).

    CAS  Google Scholar 

  50. Hu, D. et al. Increase in iron-bound organic carbon content under simulated sea-level rise: a ‘marsh organ’ field experiment. Soil Biol. Biochem. 187, 109217 (2023).

    CAS  Google Scholar 

  51. Kirwan, M. L. & Megonigal, J. P. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504, 53–60 (2013).

    CAS  Google Scholar 

  52. Rietl, A. J., Megonigal, J. P., Herbert, E. R. & Kirwan, M. L. Vegetation type and decomposition priming mediate brackish marsh carbon accumulation under interacting facets of global change. Geophys. Res. Lett. 48, e2020GL092051 (2021).

    CAS  Google Scholar 

  53. van Breemen, N. How Sphagnum bogs down other plants. Trends Ecol. Evol. 10, 270–275 (1995).

    Google Scholar 

  54. Gavazov, K. et al. Vascular plant-mediated controls on atmospheric carbon assimilation and peat carbon decomposition under climate change. Glob. Chang. Biol. 24, 3911–3921 (2018).

    Google Scholar 

  55. Malhotra, A. et al. Peatland warming strongly increases fine-root growth. Proc. Natl Acad. Sci. USA 117, 17627–17634 (2020).

    CAS  Google Scholar 

  56. Norby, R. J., Childs, J., Hanson, P. J. & Warren, J. M. Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog. Ecol. Evol. 9, 12571–12585 (2019).

    Google Scholar 

  57. Spivak, A. C., Sanderman, J., Bowen, J. L., Canuel, E. A. & Hopkinson, C. S. Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems. Nat. Geosci. 12, 685–692 (2019).

    CAS  Google Scholar 

  58. Kaštovská, E., Cardenas-Hernandez, J. & Kuzyakov, Y. Priming effects in the rhizosphere and root detritusphere of two wet-grassland graminoids. Plant Soil 472, 105–126 (2022).

    Google Scholar 

  59. Linkosalmi, M. et al. Studying the impact of living roots on the decomposition of soil organic matter in two different forestry-drained peatlands. Plant Soil 396, 59–72 (2015).

    CAS  Google Scholar 

  60. Walker, T. N. et al. Vascular plants promote ancient peatland carbon loss with climate warming. Glob. Chang. Biol. 22, 1880–1889 (2016).

    Google Scholar 

  61. Rohatgi, A. WebPlotDigitizer v.4.5 (Automeris, 2021); https://automeris.io/WebPlotDigitizer

  62. Nakagawa, S. et al. A robust and readily implementable method for the meta-analysis of response ratios with and without missing standard deviations. Ecol. Lett. 26, 232–244 (2023).

    Google Scholar 

  63. Bernal, B., Megonigal, J. P. & Mozdzer, T. J. An invasive wetland grass primes deep soil carbon pools. Glob. Chang. Biol. 23, 2104–2116 (2017).

    Google Scholar 

  64. Mozdzer, T. J., Langley, J. A., Mueller, P. & Megonigal, J. P. Deep rooting and global change facilitate spread of invasive grass. Biol. Invasions 18, 2619–2631 (2016).

    Google Scholar 

  65. Yan, W., Wang, Y., Ju, P., Huang, X. & Chen, H. Water level regulates the rhizosphere priming effect on SOM decomposition of peatland soil. Rhizosphere 21, 100455 (2022).

    Google Scholar 

  66. Zhu, Z. et al. Rice rhizodeposits affect organic matter priming in paddy soil: the role of N fertilization and plant growth for enzyme activities, CO2 and CH4 emissions. Soil Biol. Biochem. 116, 369–377 (2018).

    CAS  Google Scholar 

  67. Tett, R. P., Jackson, D. N., Rothstein, M. & Reddon, J. R. Meta-analysis of bidirectional relations in personality-job performance research. Hum. Perform. 12, 1–29 (1999).

    Google Scholar 

  68. Nakagawa, S., Yang, Y., Macartney, E. L., Spake, R. & Lagisz, M. Quantitative evidence synthesis: a practical guide on meta-analysis, meta-regression and publication bias tests for environmental sciences. Environ. Evid. 12, 8 (2023).

    Google Scholar 

  69. Leberg, P. L. Estimating allelic richness: effects of sample size and bottlenecks. Mol. Ecol. 11, 2445–2449 (2002).

    CAS  Google Scholar 

  70. Nipperess, D. A. & Matsen, F. A. The mean and variance of phylogenetic diversity under rarefaction. Methods Ecol. Evol. 4, 566–572 (2013).

    Google Scholar 

  71. Wang, H., Richardson, C. J. & Ho, M. Dual controls on carbon loss during drought in peatlands. Nat. Clim. Chang. 5, 584–587 (2015).

    CAS  Google Scholar 

  72. Reid, J. B. & Goss, M. J. Interactions between soil drying due to plant water use and decreases in aggregate stability caused by maize roots. J. Soil Sci. 33, 47–53 (1982).

    Google Scholar 

  73. Dacey, J. W. H. & Howes, B. L. Water uptake by roots controls water table movement and sediment oxidation in short Spartina marsh. Science 224, 487–489 (1984).

    CAS  Google Scholar 

  74. Birch, H. F. The effect of soil drying on humus decomposition and nitrogen availability. Plant Soil 10, 9–31 (1958).

    CAS  Google Scholar 

  75. Fenner, N. & Freeman, C. Drought-induced carbon loss in peatlands. Nat. Geosci. 4, 895–900 (2011).

    CAS  Google Scholar 

  76. Wang, X. & Tang, C. The role of rhizosphere pH in regulating the rhizosphere priming effect and implications for the availability of soil-derived nitrogen to plants. Ann. Bot. 121, 143–151 (2018).

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  78. Ren, L., Jensen, K., Porada, P. & Mueller, P. Biota-mediated carbon cycling—a synthesis of biotic-interaction controls on blue carbon. Ecol. Lett. 25, 521–540 (2022).

    Google Scholar 

Download references

Acknowledgements

This research was funded through the DFG (Deutsche Forschungsgemeinschaft) Emmy Noether Program (502681570), the National Science Foundation Long-Term Research in Environmental Biology Program (DEB-0950080, DEB-1457100, DEB-1557009 and DEB-2051343), the Department of Energy Terrestrial Ecosystem Science Program (DE-FG02-97ER62458, DE-SC0014413, DE-SC0019110 and DE-SC0021112), the Department of Energy Environmental System Science Program through the COMPASS-FME project (DE-AC05-76RL01830), the United States Geological Survey (G10AC00675) and the Smithsonian Institution.

Author information

Authors and Affiliations

Authors

Contributions

P.M. and J.P.M. conceived the study. P.M. conducted the literature survey and meta-analysis. P.M. and J.P.M. wrote the paper in equal shares.

Corresponding authors

Correspondence to Peter Mueller or J. Patrick Megonigal.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Geoscience thanks Joel Kostka, Yakov Kuzyakov and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2, and Figs. 1 and 2.

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

Mueller, P., Megonigal, J.P. Redox control on rhizosphere priming in wetlands. Nat. Geosci. 17, 1209–1217 (2024). https://doi.org/10.1038/s41561-024-01584-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41561-024-01584-1

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