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Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria

Jean-Baptiste Raina Orcid Logo, Marco Giardina, Douglas R. Brumley Orcid Logo, Peta L. Clode Orcid Logo, Mathieu Pernice Orcid Logo, Paul Guagliardo Orcid Logo, Jeremy Bougoure, Himasha Mendis, Steven Smriga, Eva C. Sonnenschein Orcid Logo, Matthias S. Ullrich, Roman Stocker Orcid Logo, Justin R. Seymour Orcid Logo

Nature Microbiology, Volume: 8, Issue: 3, Pages: 510 - 521

Swansea University Author: Eva C. Sonnenschein Orcid Logo

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DOI (Published version): 10.1038/s41564-023-01327-9

Abstract

Behaviours such as chemotaxis can facilitate metabolic exchanges between phytoplankton and heterotrophic bacteria, which ultimately regulate oceanic productivity and biogeochemistry. However, numerically dominant picophytoplankton have been considered too small to be detected by chemotactic bacteria...

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Published in: Nature Microbiology
ISSN: 2058-5276
Published: Springer Science and Business Media LLC 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa62673
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spelling v2 62673 2023-02-16 Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria f6a4027578a15ea3e6453a54b849c686 0000-0001-6959-5100 Eva C. Sonnenschein Eva C. Sonnenschein true false 2023-02-16 BGPS Behaviours such as chemotaxis can facilitate metabolic exchanges between phytoplankton and heterotrophic bacteria, which ultimately regulate oceanic productivity and biogeochemistry. However, numerically dominant picophytoplankton have been considered too small to be detected by chemotactic bacteria, implying that cell–cell interactions might not be possible between some of the most abundant organisms in the ocean. Here we examined how bacterial behaviour influences metabolic exchanges at the single-cell level between the ubiquitous picophytoplankton Synechococcus and the heterotrophic bacterium Marinobacter adhaerens, using bacterial mutants deficient in motility and chemotaxis. Stable-isotope tracking revealed that chemotaxis increased nitrogen and carbon uptake of both partners by up to 4.4-fold. A mathematical model following thousands of cells confirmed that short periods of exposure to small but nutrient-rich microenvironments surrounding Synechococcus cells provide a considerable competitive advantage to chemotactic bacteria. These findings reveal that transient interactions mediated by chemotaxis can underpin metabolic relationships among the ocean’s most abundant microorganisms. Journal Article Nature Microbiology 8 3 510 521 Springer Science and Business Media LLC 2058-5276 1 3 2023 2023-03-01 10.1038/s41564-023-01327-9 COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University Australian Research Council grant, Australian Research Council Fellowship, Simons Foundation, Gordon and Betty Moore Symbiosis in Aquatic Ecosystems Initiative Investigator Award, Swiss National Science Foundation DP180100838, FT210100100, DE180100911, 542395, GBMF9197; https://doi.org/10.37807/GBMF9197, 315230_176189 2024-07-17T08:56:33.4326622 2023-02-16T09:30:29.4132459 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Jean-Baptiste Raina 0000-0002-7508-0004 1 Marco Giardina 2 Douglas R. Brumley 0000-0003-0587-0251 3 Peta L. Clode 0000-0002-5188-4737 4 Mathieu Pernice 0000-0002-3431-2104 5 Paul Guagliardo 0000-0003-3488-6754 6 Jeremy Bougoure 7 Himasha Mendis 8 Steven Smriga 9 Eva C. Sonnenschein 0000-0001-6959-5100 10 Matthias S. Ullrich 11 Roman Stocker 0000-0002-3199-0508 12 Justin R. Seymour 0000-0002-3745-6541 13 62673__26609__da8ace12cbbc4cafb5481c363003dbeb.pdf 62673.pdf 2023-02-17T12:47:03.9979116 Output 2038674 application/pdf Accepted Manuscript true 2023-08-09T00:00:00.0000000 true eng 62673__26610__ab657acf7451471f91c7d50e727aa4e5.pdf 62673supp.pdf 2023-02-17T12:47:29.4771105 Output 329253 application/pdf Accepted Manuscript true 2023-08-09T00:00:00.0000000 Supplementary figures true eng
title Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
spellingShingle Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
Eva C. Sonnenschein
title_short Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
title_full Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
title_fullStr Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
title_full_unstemmed Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
title_sort Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
author_id_str_mv f6a4027578a15ea3e6453a54b849c686
author_id_fullname_str_mv f6a4027578a15ea3e6453a54b849c686_***_Eva C. Sonnenschein
author Eva C. Sonnenschein
author2 Jean-Baptiste Raina
Marco Giardina
Douglas R. Brumley
Peta L. Clode
Mathieu Pernice
Paul Guagliardo
Jeremy Bougoure
Himasha Mendis
Steven Smriga
Eva C. Sonnenschein
Matthias S. Ullrich
Roman Stocker
Justin R. Seymour
format Journal article
container_title Nature Microbiology
container_volume 8
container_issue 3
container_start_page 510
publishDate 2023
institution Swansea University
issn 2058-5276
doi_str_mv 10.1038/s41564-023-01327-9
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description Behaviours such as chemotaxis can facilitate metabolic exchanges between phytoplankton and heterotrophic bacteria, which ultimately regulate oceanic productivity and biogeochemistry. However, numerically dominant picophytoplankton have been considered too small to be detected by chemotactic bacteria, implying that cell–cell interactions might not be possible between some of the most abundant organisms in the ocean. Here we examined how bacterial behaviour influences metabolic exchanges at the single-cell level between the ubiquitous picophytoplankton Synechococcus and the heterotrophic bacterium Marinobacter adhaerens, using bacterial mutants deficient in motility and chemotaxis. Stable-isotope tracking revealed that chemotaxis increased nitrogen and carbon uptake of both partners by up to 4.4-fold. A mathematical model following thousands of cells confirmed that short periods of exposure to small but nutrient-rich microenvironments surrounding Synechococcus cells provide a considerable competitive advantage to chemotactic bacteria. These findings reveal that transient interactions mediated by chemotaxis can underpin metabolic relationships among the ocean’s most abundant microorganisms.
published_date 2023-03-01T08:56:33Z
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score 11.035634

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