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The microbial carbon pump and climate change

Abstract

The ocean has been a regulator of climate change throughout the history of Earth. One key mechanism is the mediation of the carbon reservoir by refractory dissolved organic carbon (RDOC), which can either be stored in the water column for centuries or released back into the atmosphere as CO2 depending on the conditions. The RDOC is produced through a myriad of microbial metabolic and ecological processes known as the microbial carbon pump (MCP). Here, we review recent research advances in processes related to the MCP, including the distribution patterns and molecular composition of RDOC, links between the complexity of RDOC compounds and microbial diversity, MCP-driven carbon cycles across time and space, and responses of the MCP to a changing climate. We identify knowledge gaps and future research directions in the role of the MCP, particularly as a key component in integrated approaches combining the mechanisms of the biological and abiotic carbon pumps for ocean negative carbon emissions.

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Fig. 1: Marine carbon cycling and the major processes and mechanisms involved.
Fig. 2: Microorganism–DOM complex networks.
Fig. 3: The MCP in changing environments.
Fig. 4: The RDOC pool driven by the MCP is a two-way regulator of climate change.
Fig. 5: Differences between the BCP, the MCP and the CCP.
Fig. 6: An integrated approach for maximum carbon sequestration in the ocean.

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References

  1. Gattuso, J.-P. et al. Ocean solutions to address climate change and its effects on marine ecosystems. Front. Mar. Sci. 5, 337 (2018).

    Article  Google Scholar 

  2. Gattuso, J.-P. & Jiao, N. Ocean-based climate actions recommended by academicians from Europe and China. Sci. China Earth Sci. 65, 1612–1614 (2022).

    Article  Google Scholar 

  3. Jiao, N. Z. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599 (2010). To our knowledge, this study is the first to propose the theory of a MCP.

    Article  CAS  PubMed  Google Scholar 

  4. Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677–680 (1979).

    Article  ADS  Google Scholar 

  5. Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Article  Google Scholar 

  6. Volk, T. & Hoffert, M. I. in The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present (eds Sundquist, E.T. & Broecker, W.S.) 99–110 (AGU, 1985).

  7. Gattuso, J. P., Frankignoulle, M. & Smith, S. V. Measurement of community metabolism and significance in the coral reef CO2 source-sink debate. Proc. Natl Acad. Sci. USA 96, 13017–13022 (1999).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Gonsior, M., Powers, L., Lahm, M. & McCallister, S. L. New perspectives on the marine carbon cycle — the marine dissolved organic matter reactivity continuum. Environ. Sci. Technol. 56, 5371–5380 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Buesseler, K. O. et al. VERTIGO (VERtical Transport in the Global Ocean): a study of particle sources and flux attenuation in the North Pacific. Deep Sea Res. II 55, 1522–1539 (2008).

    Article  ADS  Google Scholar 

  10. Falkowski, P. G., Barber, R. T. & Smetacek, V. Biogeochemical controls and feedbacks on ocean primary production. Science 281, 200–206 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. Chisholm, S. W. Stirring times in the Southern Ocean. Nature 407, 685–687 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Henson, S. A. et al. Uncertain response of ocean biological carbon export in a changing world. Nat. Geosci. 15, 248–254 (2022). This study emphasizes the uncertainty in predicting the role of the BCP in global carbon cycling.

    Article  ADS  CAS  Google Scholar 

  13. Sigman, D. M. & Boyle, E. A. Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407, 859–869 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Friedlingstein, P. et al. Global carbon budget 2022. Earth Syst. Sci. Data 14, 4811–4900 (2022).

    Article  ADS  Google Scholar 

  15. Liang, C. & Balser, T. C. Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat. Rev. Microbiol. 9, 75 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Osterholz, H. et al. Inefficient microbial production of refractory dissolved organic matter in the ocean. Nat. Commun. 6, 7422 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Wang, P. et al. Long-term cycles in the carbon reservoir of the Quaternary ocean: a perspective from the South China Sea. Natl. Sci. Rev. 1, 119–143 (2014).

    Article  CAS  Google Scholar 

  18. Hansell, D. A., Carlson, C. A. & Schlitzer, R. Net removal of major marine dissolved organic carbon fractions in the subsurface ocean. Glob. Biogeochem. Cycles 26, GB1016 (2012).

    Article  ADS  Google Scholar 

  19. Jiao, N. et al. A roadmap for ocean negative carbon emission eco-engineering in sea-farming fields. Innov. Geosci. 1, 100029 (2023). This study describes a road map for the ONCE eco-engineering approach.

    Article  Google Scholar 

  20. Karl, D. M. Microbiological oceanography — hidden in a sea of microbes. Nature 415, 590–591 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Ogawa, H. & Tanoue, E. Dissolved organic matter in oceanic waters. J. Oceanogr. 59, 129–147 (2003).

    Article  CAS  Google Scholar 

  22. Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).

    Article  ADS  Google Scholar 

  23. Dittmar, T. et al. Enigmatic persistence of dissolved organic matter in the ocean. Nat. Rev. Earth Env. 2, 570–583 (2021). This article overviews the theories on the long-term persistence of marine dissolved organic matter.

    Article  CAS  Google Scholar 

  24. Jiao, N. et al. Unveiling the enigma of refractory carbon in the ocean. Natl Sci. Rev. 5, 459–463 (2018).

    Article  CAS  Google Scholar 

  25. He, C. et al. Metagenomic evidence for the microbial transformation of carboxyl-rich alicyclic molecules: a long-term macrocosm experiment. Water Res. 216, 118281 (2022). This study highlights the potential relationship between RDOC and microbial metabolism.

    Article  CAS  PubMed  Google Scholar 

  26. Fike, D. A., Grotzinger, J. P., Pratt, L. M. & Summons, R. E. Oxidation of the Ediacaran ocean. Nature 444, 744–747 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Rothman, D. H., Hayes, J. M. & Summons, R. E. Dynamics of the neoproterozoic carbon cycle. Proc. Natl Acad. Sci. USA 100, 8124–8129 (2003).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. Schwalbach, M. S. et al. The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ. Microbiol. 12, 490–500 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Wells, L. E. & Deming, J. W. Significance of bacterivory and viral lysis in bottom waters of Franklin Bay, Canadian Arctic, during winter. Aquat. Microb. Ecol. 43, 209–221 (2006).

    Article  Google Scholar 

  30. Jiao, N. et al. Mechanisms of microbial carbon sequestration in the ocean future research directions. Biogeosciences 11, 5285–5306 (2014).

    Article  ADS  Google Scholar 

  31. Arrieta, J. M. et al. Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348, 331–333 (2015). This study supports the dilution hypothesis to explain DOC consumption by microorganisms in the deep ocean.

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Shen, Y. & Benner, R. Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean. Limnol. Oceanogr. 65, 1061–1071 (2020).

    Article  ADS  CAS  Google Scholar 

  33. Jiao, N. et al. Comment on “Dilution limits dissolved organic carbon utilization in the deep ocean”. Science 350, 148 (2015).

    Article  Google Scholar 

  34. Lennartz, S. T. & Dittmar, T. Controls on turnover of marine dissolved organic matter — testing the null hypothesis of purely concentration-driven uptake: comment on Shen and Benner, “Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean”. Limnol. Oceanogr. 67, 673–679 (2022).

    Article  ADS  Google Scholar 

  35. Wang, N. et al. Contribution of structural recalcitrance to the formation of the deep oceanic dissolved organic carbon reservoir. Environ. Microbiol. Rep. 10, 711–717 (2018).

    Article  CAS  PubMed  Google Scholar 

  36. Jiao, N. Carbon fixation and sequestration in the ocean, with special reference to the microbial carbon pump (in Chinese). Sci. Sin. Terrae 42, 1473–1486 (2012).

    Google Scholar 

  37. Jiao, N. et al. Why productive upwelling areas are often sources rather than sinks of CO2? — A comparative study on eddy upwellings in the South China Sea. Biogeosci. Discuss. 10, 13399–13426 (2013).

    ADS  Google Scholar 

  38. Jiao, N., Wang, H., Xu, G. & Aricò, S. Blue carbon on the rise: challenges and opportunities. Natl Sci. Rev. 5, 464–468 (2018).

    Article  Google Scholar 

  39. Hopkinson, C. S. & Vallino, J. J. Efficient export of carbon to the deep ocean through dissolved organic matter. Nature 433, 142–145 (2005).

    Article  ADS  CAS  PubMed  Google Scholar 

  40. Pachiadaki, M. G. et al. Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation. Science 358, 1046–1050 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  41. Hansell, D. A. Recalcitrant dissolved organic carbon fractions. Annu. Rev. Mar. Sci. 5, 421–445 (2013). This study presents a detailed description of recalcitrant DOC fractions.

    Article  Google Scholar 

  42. Bauer, J. E., Williams, P. M. & Druffel, E. R. M. C-14 activity of dissolved organic-carbon fractions in the North-Central Pacific and Sargasso Sea. Nature 357, 667–670 (1992).

    Article  ADS  CAS  Google Scholar 

  43. Druffel, E. R. M. et al. Dissolved organic radiocarbon in the central Pacific ocean. Geophys. Res. Lett. 46, 5396–5403 (2019).

    Article  ADS  CAS  Google Scholar 

  44. Follett, C. L. et al. Hidden cycle of dissolved organic carbon in the deep ocean. Proc. Natl Acad. Sci. USA 111, 16706–16711 (2014).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  45. McCarthy, M. D. et al. Chemosynthetic origin of C-14-depleted dissolved organic matter in a ridge-flank hydrothermal system. Nat. Geosci. 4, 32–36 (2011).

    Article  ADS  CAS  Google Scholar 

  46. White, M. E. et al. Refractory dissolved organic matter has similar chemical characteristics but different radiocarbon signatures with depth in the marine water column. Glob. Biogeochem. Cycles 37, e2022GB007603 (2023).

    Article  ADS  CAS  Google Scholar 

  47. Baltar, F. et al. What is refractory organic matter in the ocean? Front. Mar. Sci. 8, 642637 (2021).

    Article  Google Scholar 

  48. Zhao, Z. et al. Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties. Nat. Commun. 8, 15284 (2017).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  49. Shimotori, K., Omori, Y. & Hama, T. Bacterial production of marine humic-like fluorescent dissolved organic matter and its biogeochemical importance. Aquat. Microb. Ecol. 58, 55–66 (2009).

    Article  Google Scholar 

  50. Paerl, R. W. et al. Dityrosine formation via reactive oxygen consumption yields increasingly recalcitrant humic-like fluorescent organic matter in the ocean. Limnol. Oceanogr. Lett. 5, 331–378 (2020).

    Article  Google Scholar 

  51. Zheng, Q. et al. Molecular characteristics of microbially mediated transformations of Synechococcus-derived dissolved organic matter as revealed by incubation experiments. Environ. Microbiol. 21, 2533–2543 (2019).

    Article  CAS  PubMed  Google Scholar 

  52. Hansen, A. M. et al. Optical properties of dissolved organic matter (DOM): effects of biological and photolytic degradation. Limnol. Oceanogr. 61, 1015–1032 (2016).

    Article  ADS  Google Scholar 

  53. Xiao, X., Yamashita, Y., Gonsior, M. & Jiao, N. The efficiency of the microbial carbon pump as seen from the relationship between apparent oxygen utilization and fluorescent dissolved organic matter. Prog. Oceanogr. 210, 102929 (2023).

    Article  Google Scholar 

  54. Cai, R. et al. Microbial processing of sediment-derived dissolved organic matter: implications for its subsequent biogeochemical cycling in overlying seawater. J. Geophys. Res. Biogeosci. 124, 3479–3490 (2019).

    Article  ADS  CAS  Google Scholar 

  55. Hertkorn, N. et al. Characterization of a major refractory component of marine dissolved organic matter. Geochim. Cosmochim. Acta 70, 2990–3010 (2006).

    Article  ADS  CAS  Google Scholar 

  56. Hertkorn, N. et al. High-field NMR spectroscopy and FTICR mass spectrometry: powerful discovery tools for the molecular level characterization of marine dissolved organic matter. Biogeosciences 10, 1583–1624 (2013).

    Article  ADS  CAS  Google Scholar 

  57. Seidel, M., Vemulapalli, S. P. B., Mathieu, D. & Dittmar, T. Marine dissolved organic matter shares thousands of molecular formulae yet differs structurally across major water masses. Environ. Sci. Technol. 56, 3758–3769 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  58. Lian, J. et al. Microbial transformation of distinct exogenous substrates into analogous composition of recalcitrant dissolved organic matter. Environ. Microbiol. 23, 2333–2705 (2021).

    Article  Google Scholar 

  59. Liu, Y. et al. Epiphytic bacteria are essential for the production and transformation of algae-derived carboxyl-rich alicyclic molecule (CRAM)-like DOM. Microbiol. Spectr. 9, e0153121 (2021).

    Article  PubMed  Google Scholar 

  60. Che, J. et al. Linking microbial community structure with molecular composition of dissolved organic matter during an industrial-scale composting. J. Hazard. Mater. 405, 124281 (2021).

    Article  CAS  PubMed  Google Scholar 

  61. Zhang, Y. et al. Decreasing molecular diversity of soil dissolved organic matter related to microbial community along an alpine elevation gradient. Sci. Total. Environ. 818, 151823 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  62. Lechtenfeld, O. J. et al. Marine sequestration of carbon in bacterial metabolites. Nat. Commun. 6, 6711 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  63. Liu, S. T. et al. Different carboxyl-rich alicyclic molecules proxy compounds select distinct bacterioplankton for oxidation of dissolved organic matter in the mesopelagic Sargasso Sea. Limnol. Oceanogr. 65, 1532–1553 (2020).

    Article  ADS  CAS  Google Scholar 

  64. Dittmar, T., Koch, B., Hertkorn, N. & Kattner, G. A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnol. Oceanogr. Meth. 6, 230–235 (2008).

    Article  CAS  Google Scholar 

  65. Yamashita, Y. et al. Fate of dissolved black carbon in the deep Pacific Ocean. Nat. Commun. 13, 307 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  66. Bostick, K. W. et al. Biolability of fresh and photodegraded pyrogenic dissolved organic matter from laboratory-prepared chars. J. Geophys. Res. Biogeosci. 126, e2020JG005981 (2021).

    Article  ADS  CAS  Google Scholar 

  67. Coppola, A. I. et al. The black carbon cycle and its role in the Earth system. Nat. Rev. Earth Env. 3, 516–532 (2022).

    Article  CAS  Google Scholar 

  68. Santin, C. et al. Towards a global assessment of pyrogenic carbon from vegetation fires. Glob. Change Biol. 22, 76–91 (2016).

    Article  ADS  Google Scholar 

  69. Wagner, S., Jaffe, R. & Stubbins, A. Dissolved black carbon in aquatic ecosystems. Limnol. Oceanogr. Lett. 3, 168–185 (2018).

    Article  CAS  Google Scholar 

  70. Wagner, S. et al. Isotopic composition of oceanic dissolved black carbon reveals non-riverine source. Nat. Commun. 10, 5064 (2019).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  71. Luther, G. W. Hydrothermal vents are a source of old refractory organic carbon to the deep ocean. Geophys. Res. Lett. 48, e2021GL09486 (2021).

    Article  Google Scholar 

  72. Yamashita, Y., Mori, Y. & Ogawa, H. Hydrothermal-derived black carbon as a source of recalcitrant dissolved organic carbon in the ocean. Sci. Adv. 9, eade3807 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  73. Coppola, A. I. & Druffel, E. R. M. Cycling of black carbon in the ocean. Geophys. Res. Lett. 43, 4477–4482 (2016).

    Article  ADS  CAS  Google Scholar 

  74. Wang, Y. et al. Linking microbial population succession and DOM molecular changes in Synechococcus-derived organic matter addition incubation. Microbiol. Spectr. 10, e0230821 (2022).

    Article  PubMed  Google Scholar 

  75. LaBrie, R. et al. Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes. Sci. Adv. 8, eabn0035 (2022).

    Article  CAS  PubMed  Google Scholar 

  76. Arnosti, C. Microbial extracellular enzymes and the marine carbon cycle. Annu. Rev. Mar. Sci. 3, 401–425 (2011).

    Article  ADS  Google Scholar 

  77. Carlson, C. A. et al. Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol. Oceanogr. 49, 1073–1083 (2004).

    Article  ADS  CAS  Google Scholar 

  78. Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).

    Article  PubMed  Google Scholar 

  79. Sichert, A. et al. Verrucomicrobia use hundreds of enzymes to digest the algal polysaccharide fucoidan. Nat. Microbiol. 5, 1026–1039 (2020).

    Article  CAS  PubMed  Google Scholar 

  80. Teeling, H. et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  81. Ogawa, H. et al. Production of refractory dissolved organic matter by bacteria. Science 292, 917–920 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  82. Zheng, Q. et al. Highly enriched N-containing organic molecules of Synechococcus lysates and their rapid transformation by heterotrophic bacteria. Limnol. Oceanogr. 66, 335–348 (2021).

    Article  ADS  CAS  Google Scholar 

  83. Ma, J. et al. Carotenoid biomarkers in Namibian shelf sediments: anoxygenic photosynthesis during sulfide eruptions in the Benguela Upwelling System. Proc. Natl Acad. Sci. USA 118, e2106040118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Arakawa, N. et al. Carotenoids are the likely precursor of a significant fraction of marine dissolved organic matter. Sci. Adv. 3, e1602976 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  85. Osterholz, H. et al. Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system. ISME J. 10, 1717–1730 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Hu, A. et al. Ecological networks of dissolved organic matter and microorganisms under global change. Nat. Commun. 13, 3600 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  87. Zhao, Z. et al. Microbial transformation of virus-induced dissolved organic matter from picocyanobacteria: coupling of bacterial diversity and DOM chemodiversity. ISME J. 13, 2551–2565 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zhang, C. et al. Evolving paradigms in biological carbon cycling in the ocean. Natl. Sci. Rev. 5, 481–499 (2018).

    Article  CAS  Google Scholar 

  89. Chen, Q. et al. Correspondence between DOM molecules and microbial community in a subtropical coastal estuary on a spatiotemporal scale. Environ. Int. 154, 106558 (2021).

    Article  CAS  PubMed  Google Scholar 

  90. Chen, X. X. et al. Niche differentiation of microbial community shapes vertical distribution of recalcitrant dissolved organic matter in deep-sea sediments. Environ. Int. 178, 108080 (2023).

    Article  CAS  PubMed  Google Scholar 

  91. Bianchi, T. S. The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc. Natl Acad. Sci. USA 108, 19473–19481 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  92. Jiao, N., Tang, K., Cai, H. & Mao, Y. Increasing the microbial carbon sink in the sea by reducing chemical fertilization on the land. Nat. Rev. Microbiol. 9, 75 (2011).

    Article  CAS  Google Scholar 

  93. Dai, M. et al. Carbon fluxes in the coastal ocean: synthesis, boundary processes and future trends. Annu. Rev. Earth Planet. Sci. 50, 593–626 (2022).

    Article  ADS  CAS  Google Scholar 

  94. Dang, H. & Jiao, N. Perspectives on the microbial carbon pump with special reference to microbial respiration and ecosystem efficiency in large estuarine systems. Biogeosciences 11, 3887–3898 (2014).

    Article  ADS  Google Scholar 

  95. Liu, J., Jiao, N. & Tang, K. An experimental study on the effects of nutrient enrichment on organic carbon persistence in the western Pacific oligotrophic gyre. Biogeosciences 11, 5115–5122 (2014).

    Article  ADS  Google Scholar 

  96. Zhang, K. et al. Influence of eco-substrate addition on organic carbon, nitrogen and phosphorus budgets of intensive aquaculture ponds of the Pearl River, China. Aquaculture 520, 734868 (2020).

    Article  CAS  Google Scholar 

  97. Yuan, X. et al. Bacterial influence on chromophoric dissolved organic matter in two coastal waters of the northern South China Sea. Aquat. Microb. Ecol. 76, 207–217 (2015).

    Article  Google Scholar 

  98. Chen, X. et al. Oxygen availability driven trends in DOM molecular composition and reactivity in a seasonally stratified fjord. Water Res. 220, 118690 (2022).

    Article  CAS  PubMed  Google Scholar 

  99. Li, P. et al. Stratification of dissolved organic matter in the upper 2000 m water column at the Mariana Trench. Sci. Total Environ. 668, 1222–1231 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  100. Hansell, D. A., Carlson, C. A., Repeta, D. J. & Schlitzer, R. Dissolved organic matter in the ocean a controversy stimulates new insights. Oceanography 22, 202–211 (2009).

    Article  Google Scholar 

  101. Middelburg, J. J. Unified prediction of organic matter preservation and degradation. Commun. Earth Environ. 4, 17 (2023).

    Article  ADS  Google Scholar 

  102. Jessen, G. L. et al. Hypoxia causes preservation of labile organic matter and changes seafloor microbial community composition (Black Sea). Sci. Adv. 3, e1601897 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  103. Xiao, S. et al. Molecular characterization of organic matter transformation mediated by microorganisms under anoxic/hypoxic conditions. Sci. China Earth Sci 66, 894–909 (2023).

    Article  ADS  CAS  Google Scholar 

  104. Chen, Q. R., Tang, K., Chen, X. F. & Jiao, N. Z. Microbial sulfurization stimulates carbon sequestration in marine oxygen minimum zones. Sci. Bull. 67, 895–898 (2022).

    Article  CAS  Google Scholar 

  105. Gomez-Saez, G. V. et al. Sulfurization of dissolved organic matter in the anoxic water column of the Black Sea. Sci. Adv. 7, eabf6199 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  106. Wohlers, J. et al. Changes in biogenic carbon flow in response to sea surface warming. Proc. Natl Acad. Sci. USA 106, 7067–7072 (2009).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  107. Zhang, Y. et al. Nitrifier adaptation to low energy flux controls inventory of reduced nitrogen in the dark ocean. Proc. Natl Acad. Sci. USA 117, 4823 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  108. Amano, C. et al. Limited carbon cycling due to high-pressure effects on the deep-sea microbiome. Nat. Geosci. 15, 1041–1047 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  109. Romera-Castillo, C. et al. Net additions of recalcitrant dissolved organic carbon in the deep Atlantic ocean. Glob. Biogeochem. Cycles 33, 1162–1173 (2019).

    Article  ADS  CAS  Google Scholar 

  110. Hawkes, J. A. et al. Efficient removal of recalcitrant deep-ocean dissolved organic matter during hydrothermal circulation. Nat. Geosci. 8, 856–860 (2015).

    Article  ADS  CAS  Google Scholar 

  111. Hawkes, J. A. et al. Molecular alteration of marine dissolved organic matter under experimental hydrothermal conditions. Geochim. Cosmochim. Acta 175, 68–85 (2016).

    Article  ADS  CAS  Google Scholar 

  112. Dittmar, T. & Paeng, J. A heat-induced molecular signature in marine dissolved organic matter. Nat. Geosci. 2, 175–179 (2009).

    Article  ADS  CAS  Google Scholar 

  113. McCollom, T. M., Simoneit, B. R. T. & Shock, E. L. Hydrous pyrolysis of polycyclic aromatic hydrocarbons and implications for the origin of PAH in hydrothermal petroleum. Energy Fuel 13, 401–410 (1999).

    Article  CAS  Google Scholar 

  114. Vandenbroucke, M. & Largeau, C. Kerogen origin, evolution and structure. Org. Geochem. 38, 719–833 (2007).

    Article  ADS  CAS  Google Scholar 

  115. NASEM. A Research Strategy for Ocean-Based Carbon Dioxide Removal and Sequestration (National Academies, 2021).

  116. Wang, F. et al. Technologies and perspectives for achieving carbon neutrality. Innovation 2, 100180 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Yao, W., Paytan, A. & Wortmann, U. G. Large-scale ocean deoxygenation during the paleocene-eocene thermal maximum. Science 361, 804–806 (2018).

    Article  ADS  CAS  PubMed  Google Scholar 

  118. Legendre, L. et al. The microbial carbon pump concept: potential biogeochemical significance in the globally changing ocean. Prog. Oceanogr. 134, 432–450 (2015). This study provides a comprehensive analysis of the theoretical framework of the MCP.

    Article  ADS  Google Scholar 

  119. Swanson-Hysell, N. L. et al. Cryogenian glaciation and the onset of carbon-isotope decoupling. Science 328, 608–611 (2010).

    Article  ADS  CAS  PubMed  Google Scholar 

  120. Grotzinger, J. P., Fike, D. A. & Fischer, W. W. Enigmatic origin of the largest-known carbon isotope excursion in Earth’s history. Nat. Geosci. 4, 285–292 (2011).

    Article  ADS  CAS  Google Scholar 

  121. Li, C. et al. Uncovering the spatial heterogeneity of Ediacaran carbon cycling. Geobiology 15, 211–224 (2017).

    Article  CAS  PubMed  Google Scholar 

  122. Shi, W. et al. Sulfur isotope evidence for transient marine-shelf oxidation during the Ediacaran Shuram excursion. Geology 46, 267–270 (2018).

    Article  ADS  CAS  Google Scholar 

  123. Ridgwell, A. Evolution of the ocean’s “biological pump”. Proc. Natl Acad. Sci. USA 108, 16485–16486 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  124. Peltier, W. R., Liu, Y. G. & Crowley, J. W. Snowball Earth prevention by dissolved organic carbon remineralization. Nature 450, 813–818 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  125. Shen, Y. & Benner, R. Mixing it up in the ocean carbon cycle and the removal of refractory dissolved organic carbon. Sci. Rep. 8, 2542 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  126. Chang, B. et al. A 60-Ma-long, high-resolution record of Ediacaran paleotemperature. Sci. Bull. 67, 910–913 (2022).

    Article  Google Scholar 

  127. Yang, Y. P. et al. Is the upward release of intermediate ocean heat content a possible engine for low-latitude processes? Geology 48, 579–583 (2020).

    Article  ADS  CAS  Google Scholar 

  128. Marchitto, T. et al. Marine radiocarbon evidence for the mechanism of deglacial atmospheric CO2 rise. Science 316, 1456–1459 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  129. Martínez-Botí, M. A. et al. Boron isotope evidence for oceanic carbon dioxide leakage during the last deglaciation. Nature 518, 219–222 (2015).

    Article  ADS  PubMed  Google Scholar 

  130. Clemens, S. C. & Tiedemann, R. Eccentricity forcing of Pliocene–early Pleistocene climate revealed in a marine oxygen-isotope record. Nature 385, 801–804 (1997).

    Article  ADS  CAS  Google Scholar 

  131. Ma, W., Tian, J., Li, Q. & Wang, P. Simulation of long eccentricity (400-kyr) cycle in ocean carbon reservoir during Miocene Climate Optimum: weathering and nutrient response to orbital change. Geophys. Res. Lett. 38, L10701 (2011).

    Article  ADS  Google Scholar 

  132. Zachos, J. et al. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  133. Halverson, G. P., Wade, B. P., Hurtgen, M. T. & Barovich, K. M. Neoproterozoic chemostratigraphy. Precambrian Res. 182, 337–350 (2010).

    Article  ADS  CAS  Google Scholar 

  134. McClymont, E. L. et al. Pliocene-Pleistocene evolution of sea surface and intermediate water temperatures from the southwest Pacific. Paleoceanography 31, 895–913 (2016).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  135. Shang, H. T. A generic hierarchical model of organic matter degradation and preservation in aquatic systems. Commun. Earth Environ. 4, 16 (2023).

    Article  ADS  Google Scholar 

  136. Zakem, E. J., Cael, B. B. & Levine, N. M. A unified theory for organic matter accumulation. Proc. Natl Acad. Sci. USA 118, e2016896118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Ju, A. B., Wang, H., Wang, L. Q. & Weng, Y. Application of machine learning algorithms for prediction of ultraviolet absorption spectra of chromophoric dissolved organic matter (CDOM) in seawater. Front. Mar. Sci. 10, 1065123 (2023).

    Article  Google Scholar 

  138. Mentges, A. et al. Long-term stability of marine dissolved organic carbon emerges from a neutral network of compounds and microbes. Sci. Rep. 9, 17780 (2019).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  139. Jiao, N. et al. Microbes mediated comprehensive carbon sequestration for negative emissions in the ocean. Natl. Sci. Rev. 7, 1858–1860 (2020). This study proposes that the MCP and other microbial processes are capable of regulating ONCE.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Higgins, J. A., Fischer, W. W. & Schrag, D. P. Oxygenation of the ocean and sediments: consequences for the seafloor carbonate factory. Earth Planet. Sci. Lett. 284, 25–33 (2009).

    Article  ADS  CAS  Google Scholar 

  141. Castro-Alonso, M. J. et al. Microbially induced calcium carbonate precipitation (MICP) and its potential in bioconcrete: microbiological and molecular concepts. Front. Mater. 6, 126 (2019).

    Article  ADS  Google Scholar 

  142. Thomas, H. et al. Enhanced ocean carbon storage from anaerobic alkalinity generation in coastal sediments. Biogeosciences 6, 267–274 (2009).

    Article  ADS  CAS  Google Scholar 

  143. Gately, J. A. et al. Coccolithophores and diatoms resilient to ocean alkalinity enhancement: a glimpse of hope? Sci. Adv. 9, eadg606 (2023).

    Article  Google Scholar 

  144. Smetacek, V. et al. Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487, 313–319 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  145. Zhou, L. et al. Aluminum increases net carbon fixation by marine diatoms and decreases their decomposition: evidence for the iron–aluminum hypothesis. Limnol. Oceanogr. 66, 2712–2727 (2021).

    Article  ADS  CAS  Google Scholar 

  146. Xiong, T. Q. et al. Legacy effects of late macroalgal blooms on dissolved inorganic carbon pool through alkalinity enhancement in coastal ocean. Environ. Sci. Technol. 57, 2186–2196 (2023).

    Article  ADS  CAS  PubMed  Google Scholar 

  147. Su, J. et al. Chesapeake Bay acidification buffered by spatially decoupled carbonate mineral cycling. Nat. Geosci. 13, 441–447 (2020).

    Article  ADS  CAS  Google Scholar 

  148. Yang, X. et al. Treated wastewater changes the export of dissolved inorganic carbon and its isotopic composition and leads to acidification in coastal oceans. Environ. Sci. Technol. 52, 5590–5599 (2018).

    Article  ADS  CAS  PubMed  Google Scholar 

  149. Cai, W.-J. & Jiao, N. Wastewater alkalinity addition as a novel approach for ocean negative carbon emission. Innovation 3, 100272 (2022). This study proposes that sewage alkalization increases carbon sinks.

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Ferderer, A. et al. Assessing the influence of ocean alkalinity enhancement on a coastal phytoplankton community. Biogeosciences 19, 5375–5399 (2022).

    Article  ADS  CAS  Google Scholar 

  151. Norbisrath, M. et al. Metabolic alkalinity release from large port facilities (Hamburg, Germany)and impact on coastal carbon storage. Biogeosciences 19, 5151–5165 (2022).

    Article  ADS  CAS  Google Scholar 

  152. Zhang, L. et al. Nitrifiers drive successions of particulate organic matter and microbial community composition in a starved macrocosm. Environ. Int. 157, 106776 (2021).

    Article  CAS  PubMed  Google Scholar 

  153. Xiao, X. et al. Biodegradation of terrigenous organic matter in a stratified large-volume water column: implications of the removal of terrigenous organic matter in the coastal ocean. Environ. Sci. Technol. 56, 5234–5246 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  154. Pan, Y. et al. Evaluation of the sinks and sources of atmospheric CO2 by artificial upwelling. Sci. Total Environ. 511, 692–702 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  155. Zhang, D. et al. Carbon dioxide fluxes from two typical mariculture polyculture systems in coastal China. Aquaculture 521, 735041 (2020).

    Article  CAS  Google Scholar 

  156. Zhang, C. et al. Eco-engineering approaches for ocean negative carbon emission. Sci. Bull. 6, 2564–2573 (2022).

    Article  Google Scholar 

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Acknowledgements

The authors thank the following colleagues who are involved in the UN Decade of Ocean Science for Sustainable Development programme, Global Ocean Negative Carbon Emissions (Global-ONCE), for their valuable discussions: B. Rinkevich, C. Lopez, F. Jiao, H. Kaartokallio, J.-P. Gattuso, K. Tang, M. Weinbauer, Q. Tu, Q. Zheng, R. Cai and Y. Zhang. This work is supported by the National Science Foundation of China (42188102), the Ministry of Science and Technology (MOST) ONCE project and the UNESCO-IOC, the joint PICES/ICES Working Group 46.

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Jiao, N., Luo, T., Chen, Q. et al. The microbial carbon pump and climate change. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01018-0

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