Chemotaxis shapes the microscale organization of the ocean’s microbiome

Jean-Baptiste Raina (), Bennett S. Lambert, Donovan H. Parks, Christian Rinke, Nachshon Siboni, Anna Bramucci, Martin Ostrowski, Brandon Signal, Adrian Lutz, Himasha Mendis, Francesco Rubino, Vicente I. Fernandez, Roman Stocker, Philip Hugenholtz, Gene W. Tyson and Justin R. Seymour ()
Additional contact information
Jean-Baptiste Raina: Climate Change Cluster, Faculty of Science, University of Technology Sydney
Bennett S. Lambert: Massachusetts Institute of Technology
Donovan H. Parks: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland
Christian Rinke: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland
Nachshon Siboni: Climate Change Cluster, Faculty of Science, University of Technology Sydney
Anna Bramucci: Climate Change Cluster, Faculty of Science, University of Technology Sydney
Martin Ostrowski: Climate Change Cluster, Faculty of Science, University of Technology Sydney
Brandon Signal: Climate Change Cluster, Faculty of Science, University of Technology Sydney
Adrian Lutz: Metabolomics Australia, Bio21 Institute, The University of Melbourne, Parkville
Himasha Mendis: Metabolomics Australia, Bio21 Institute, The University of Melbourne, Parkville
Francesco Rubino: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland
Vicente I. Fernandez: Department of Civil, Environmental and Geomatic Engineering, ETH Zurich
Roman Stocker: Department of Civil, Environmental and Geomatic Engineering, ETH Zurich
Philip Hugenholtz: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland
Gene W. Tyson: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland
Justin R. Seymour: Climate Change Cluster, Faculty of Science, University of Technology Sydney

Nature, 2022, vol. 605, issue 7908, 132-138

Abstract: Abstract The capacity of planktonic marine microorganisms to actively seek out and exploit microscale chemical hotspots has been widely theorized to affect ocean-basin scale biogeochemistry1–3, but has never been examined comprehensively in situ among natural microbial communities. Here, using a field-based microfluidic platform to quantify the behavioural responses of marine bacteria and archaea, we observed significant levels of chemotaxis towards microscale hotspots of phytoplankton-derived dissolved organic matter (DOM) at a coastal field site across multiple deployments, spanning several months. Microscale metagenomics revealed that a wide diversity of marine prokaryotes, spanning 27 bacterial and 2 archaeal phyla, displayed chemotaxis towards microscale patches of DOM derived from ten globally distributed phytoplankton species. The distinct DOM composition of each phytoplankton species attracted phylogenetically and functionally discrete populations of bacteria and archaea, with 54% of chemotactic prokaryotes displaying highly specific responses to the DOM derived from only one or two phytoplankton species. Prokaryotes exhibiting chemotaxis towards phytoplankton-derived compounds were significantly enriched in the capacity to transport and metabolize specific phytoplankton-derived chemicals, and displayed enrichment in functions conducive to symbiotic relationships, including genes involved in the production of siderophores, B vitamins and growth-promoting hormones. Our findings demonstrate that the swimming behaviour of natural prokaryotic assemblages is governed by specific chemical cues, which dictate important biogeochemical transformation processes and the establishment of ecological interactions that structure the base of the marine food web.

Date: 2022
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DOI: 10.1038/s41586-022-04614-3

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