Dynamic metabolic exchange governs a marine algal-bacterial interaction

Emiliania huxleyi is a model coccolithophore micro-alga that generates vast blooms in the ocean. Bacteria are not considered among the major factors influencing coccolithophore physiology. Here we show through a laboratory model system that the bacterium Phaeobacter inhibens, a well-studied member o...

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Main Authors: Einat Segev, Thomas P Wyche, Ki Hyun Kim, Jörn Petersen, Claire Ellebrandt, Hera Vlamakis, Natasha Barteneva, Joseph N Paulson, Liraz Chai, Jon Clardy, Roberto Kolter
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/17473
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author Einat Segev
Thomas P Wyche
Ki Hyun Kim
Jörn Petersen
Claire Ellebrandt
Hera Vlamakis
Natasha Barteneva
Joseph N Paulson
Liraz Chai
Jon Clardy
Roberto Kolter
author_facet Einat Segev
Thomas P Wyche
Ki Hyun Kim
Jörn Petersen
Claire Ellebrandt
Hera Vlamakis
Natasha Barteneva
Joseph N Paulson
Liraz Chai
Jon Clardy
Roberto Kolter
author_sort Einat Segev
collection DOAJ
description Emiliania huxleyi is a model coccolithophore micro-alga that generates vast blooms in the ocean. Bacteria are not considered among the major factors influencing coccolithophore physiology. Here we show through a laboratory model system that the bacterium Phaeobacter inhibens, a well-studied member of the Roseobacter group, intimately interacts with E. huxleyi. While attached to the algal cell, bacteria initially promote algal growth but ultimately kill their algal host. Both algal growth enhancement and algal death are driven by the bacterially-produced phytohormone indole-3-acetic acid. Bacterial production of indole-3-acetic acid and attachment to algae are significantly increased by tryptophan, which is exuded from the algal cell. Algal death triggered by bacteria involves activation of pathways unique to oxidative stress response and programmed cell death. Our observations suggest that bacteria greatly influence the physiology and metabolism of E. huxleyi. Coccolithophore-bacteria interactions should be further studied in the environment to determine whether they impact micro-algal population dynamics on a global scale.
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spelling doaj.art-5d38d84635704cb7a5e969c0ff7af1f22022-12-22T03:33:55ZengeLife Sciences Publications LtdeLife2050-084X2016-11-01510.7554/eLife.17473Dynamic metabolic exchange governs a marine algal-bacterial interactionEinat Segev0https://orcid.org/0000-0002-2266-1219Thomas P Wyche1Ki Hyun Kim2https://orcid.org/0000-0002-5285-9138Jörn Petersen3Claire Ellebrandt4Hera Vlamakis5Natasha Barteneva6Joseph N Paulson7Liraz Chai8Jon Clardy9https://orcid.org/0000-0003-0213-8356Roberto Kolter10https://orcid.org/0000-0001-9548-1481Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United StatesDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United StatesDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United StatesLeibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, GermanyLeibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, GermanyDepartment of Microbiology and Immunobiology, Harvard Medical School, Boston, United StatesProgram in Cellular and Molecular Medicine, Boston Children's Hospital, Harvard Medical School, Boston, United StatesDepartment of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, United StatesDepartment of Microbiology and Immunobiology, Harvard Medical School, Boston, United StatesDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United StatesDepartment of Microbiology and Immunobiology, Harvard Medical School, Boston, United StatesEmiliania huxleyi is a model coccolithophore micro-alga that generates vast blooms in the ocean. Bacteria are not considered among the major factors influencing coccolithophore physiology. Here we show through a laboratory model system that the bacterium Phaeobacter inhibens, a well-studied member of the Roseobacter group, intimately interacts with E. huxleyi. While attached to the algal cell, bacteria initially promote algal growth but ultimately kill their algal host. Both algal growth enhancement and algal death are driven by the bacterially-produced phytohormone indole-3-acetic acid. Bacterial production of indole-3-acetic acid and attachment to algae are significantly increased by tryptophan, which is exuded from the algal cell. Algal death triggered by bacteria involves activation of pathways unique to oxidative stress response and programmed cell death. Our observations suggest that bacteria greatly influence the physiology and metabolism of E. huxleyi. Coccolithophore-bacteria interactions should be further studied in the environment to determine whether they impact micro-algal population dynamics on a global scale.https://elifesciences.org/articles/17473Emiliania huxleyiRoseobacter groupPhaeobacter inhibenssymbiosisIndole-3-acetic acidprogrammed cell death
spellingShingle Einat Segev
Thomas P Wyche
Ki Hyun Kim
Jörn Petersen
Claire Ellebrandt
Hera Vlamakis
Natasha Barteneva
Joseph N Paulson
Liraz Chai
Jon Clardy
Roberto Kolter
Dynamic metabolic exchange governs a marine algal-bacterial interaction
eLife
Emiliania huxleyi
Roseobacter group
Phaeobacter inhibens
symbiosis
Indole-3-acetic acid
programmed cell death
title Dynamic metabolic exchange governs a marine algal-bacterial interaction
title_full Dynamic metabolic exchange governs a marine algal-bacterial interaction
title_fullStr Dynamic metabolic exchange governs a marine algal-bacterial interaction
title_full_unstemmed Dynamic metabolic exchange governs a marine algal-bacterial interaction
title_short Dynamic metabolic exchange governs a marine algal-bacterial interaction
title_sort dynamic metabolic exchange governs a marine algal bacterial interaction
topic Emiliania huxleyi
Roseobacter group
Phaeobacter inhibens
symbiosis
Indole-3-acetic acid
programmed cell death
url https://elifesciences.org/articles/17473
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