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Biogeochemistry of Earth before exoenzymes

Nature Geoscience volume 16, pages 845–850 (2023)Cite this article

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Abstract

Microorganisms that transform and oxidize organic material (that is, heterotrophs) play a fundamental role in the geochemical cycling of key elements in the ocean. Through their growth and activity, heterotrophic microorganisms degrade much of the organic matter produced by phytoplankton in the surface ocean, leading to the regeneration and redistribution of nutrients and carbon back into the water column. However, most organic matter is physically too large to be taken up directly by heterotrophic microorganisms. Consequently, many heterotrophs secrete exoenzymes that break down large molecules outside the cell into smaller substrates that can then be directly taken up by the cell. The complex nature of the biochemical systems that microorganisms use to secrete these enzymes suggests that they were unlikely to have been present in the earliest heterotrophs. In a pre-exoenzyme ocean, heterotrophic microorganisms would only be able to access a small fraction of organic matter such that most dead phytoplankton biomass would have passed directly through the water column and settled onto the seafloor. Here we synthesize existing geobiological evidence to examine the fate of organic matter in the absence of exoenzymes in early oceans. We propose that on an Earth before exoenzymes, organic matter preservation, metal availability and phosphorus recycling would have operated differently than they do on the contemporary Earth.

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Fig. 1: Emergence of known heterotrophic and autotrophic metabolic processes in the early oceans that may have given rise to exoenzymes.
Fig. 2: Important exoenzyme-mediated, abiotic and biotic processes in the early oceans.

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Acknowledgements

This research was supported financially by Natural Sciences & Engineering Research Council of Canada (NSERC) grants to K.O.K. (RGPIN-2020-05189) and G.P.H. N.M. was supported by a New Frontiers in Research Fund Exploration Grant (NFRFE-2019-00794). A.D.S. was supported by NSF grant numbers OPP-2147046 and OCE- 2145434. We thank A. Grossman for helpful conversations about enzyme secretion systems.

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Authors and Affiliations

  1. Department of Earth & Planetary Sciences, McGill University, Montreal, Quebec, Canada

    Nagissa Mahmoudi & Galen P. Halverson

  2. Departments of Microbiology and Earth and Planetary Sciences, University of Tennessee, Knoxville, TN, USA

    Andrew D. Steen

  3. Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada

    Kurt O. Konhauser

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  1. Nagissa Mahmoudi
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N.M. and A.D.S conceptualized the Perspective. All authors extensively contributed ideas and provided critical feedback in the research, interpretation and writing.

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Correspondence to Nagissa Mahmoudi.

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Mahmoudi, N., Steen, A.D., Halverson, G.P. et al. Biogeochemistry of Earth before exoenzymes. Nat. Geosci. 16, 845–850 (2023). https://doi.org/10.1038/s41561-023-01266-4

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