Constraining the oxygen requirements for modern microbial eukaryote diversity

Author:

Mills Daniel B.123ORCID,Simister Rachel L.4,Sehein Taylor R.5,Hallam Steven J.46789,Sperling Erik A.2ORCID,Crowe Sean A.410

Affiliation:

1. Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig-Maximilians-Universität München, 80333 Munich, Germany

2. Department of Earth and Planetary Sciences, Stanford University, Stanford, CA 94305

3. The Penn State Extraterrestrial Intelligence Center, The Pennsylvania State University, University Park, PA 16802

4. Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

5. Department of Biological Sciences, Smith College, Northampton, MA 01063

6. Genome Science and Technology Program, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

7. Graduate Program in Bioinformatics, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

8. Life Sciences Institute, University of British Columbia, Vancouver, BC V6T 1Z3, Canada

9. Bradshaw Research Initiative for Minerals and Mining, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

10. Department of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

Abstract

Eukaryotes originated prior to the establishment of modern marine oxygen (O 2 ) levels. According to the body fossil and lipid biomarker records, modern (crown) microbial eukaryote lineages began diversifying in the ocean no later than ~800 Ma. While it has long been predicted that increasing atmospheric O 2 levels facilitated the early diversification of microbial eukaryotes, the O 2 levels needed to permit this diversification remain unconstrained. Using time-resolved geochemical parameter and gene sequence information from a model marine oxygen minimum zone spanning a range of dissolved O 2 levels and redox states, we show that microbial eukaryote taxonomic richness and phylogenetic diversity remain the same until O 2 declines to around 2 to 3% of present atmospheric levels, below which these diversity metrics become significantly reduced. Our observations suggest that increasing O 2 would have only directly promoted early crown-eukaryote diversity if atmospheric O 2 was below 2 to 3% of modern levels when crown-eukaryotes originated and then later met or surpassed this range as crown-eukaryotes diversified. If atmospheric O 2 was already consistently at or above 2 to 3% of modern levels by the time that crown-eukaryotes originated, then the subsequent diversification of modern microbial eukaryotes was not directly driven by atmospheric oxygenation.

Funder

Agouron Institute

Deutsche Forschungsgemeinschaft

Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada

Publisher

Proceedings of the National Academy of Sciences

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