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Volume 68, Issue 7 p. 1417-1437
Review

Do phytoplankton require oxygen to survive? A hypothesis and model synthesis from oxygen minimum zones

Jane C. Y. Wong

Corresponding Author

Jane C. Y. Wong

Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile

Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

Correspondence: [email protected] and [email protected]

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John A. Raven

John A. Raven

Division of Plant Science, University of Dundee at the James Hutton Institute, Dundee, UK

School of Biological Sciences, University of Western Australia, Crawley, Western Australia, Australia

Climate Change Cluster, Faculty of Science, University of Technology Sydney, Sydney, New South Wales, Australia

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Montserrat Aldunate

Montserrat Aldunate

Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile

Coastal Ecosystems and Global Environmental Change Lab (ECCA Lab), Department of Aquatic System, Faculty of Environmental Sciences, Universidad de Concepcion, Chile

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Sebastián Silva

Sebastián Silva

Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany

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Juan Diego Gaitán-Espitia

Juan Diego Gaitán-Espitia

School of Biological Sciences and The Swire Institute of Marine Sciences, The University of Hong Kong, Hong Kong, China

Institute for Climate and Carbon Neutrality, The University of Hong Kong, Hong Kong, China

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Cristian A. Vargas

Cristian A. Vargas

Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile

Coastal Ecosystems and Global Environmental Change Lab (ECCA Lab), Department of Aquatic System, Faculty of Environmental Sciences, Universidad de Concepcion, Chile

Coastal Social-Ecological Millennium Institute (SECOS), Universidad de Concepcion, Concepcion, Chile

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Osvaldo Ulloa

Osvaldo Ulloa

Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile

Departamento de Oceanografía, Universidad de Concepción, Concepción, Chile

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Peter von Dassow

Corresponding Author

Peter von Dassow

Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile

Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Naples, Italy

Correspondence: [email protected] and [email protected]

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First published: 07 May 2023

Author Contribution Statement: J.C.Y.W., J.D.G.E. and P.D. conceptualized the research. M.A., S.S. and C.A.V. provided study materials and cruise data. J.C.Y.W., M.A., S.S., O.U. and P.D. contributed data analysis and modeling tools. J.C.Y.W., J.A.R. and P.D. prepared the original draft. All authors revised and approved the final version.

Associate editor: Laura Bristow

Abstract

It is commonly known that phytoplankton have a pivotal role in marine biogeochemistry and ecosystems as carbon fixers and oxygen producers, but their response to deoxygenation has scarcely been studied. Nonetheless, in the major oceanic oxygen minimum zones (OMZs), all surface phytoplankton groups, regardless of size, disappear and are replaced by unique cyanobacteria lineages below the oxycline. To develop reasonable hypotheses to explain this pattern, we conduct a review of available information on OMZ phytoplankton, and we re-analyze previously published data (flow cytometric and hydrographic) on vertical structure of phytoplankton communities in relation to light and O2 levels. We also review the physical constraints on O2 acquisition as well as O2-dependent metabolisms in phototrophs. These considerations, along with estimates of the photosynthetic capacity of phytoplankton along OMZ depth profiles using published data, suggest that top-down grazing, respiratory demand, and irradiance are insufficient to fully explain the vertical structure observed in the upper, more sunlit portions of OMZs. Photorespiration and water–water cycles are O2-dependent pathways with low O2 affinities. Although their metabolic roles are still poorly understood, a hypothetical dependence on such pathways by the phytoplankton adapted to the oxic ocean might explain vertical patterns in OMZs and results of laboratory experiments. This can be represented in a simple model in which the requirement for photorespiration in surface phytoplankton and O2-inhibition of OMZ lineages reproduces the observed vertical fluorescence profiles and the replacement of phytoplankton adapted to O2 by lineages restricted to the most O2-deficient waters. A high O2 requirement by modern phytoplankton would suggest a positive feedback that intensifies trends in OMZ extent and ocean oxygenation or deoxygenation, both in Earth's past and in response to current climate change.

Conflict of Interest

None declared.

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article and/or its supplementary materials.