Dynamic metabolic exchange governs a marine algal-bacterial interaction

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

doi:10.7554/eLife.17473

Dynamic metabolic exchange governs a marine algal-bacterial interaction

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

Harvard University
Sungkyunkwan University
German Collection of Microorganisms and Cell Cultures
Broad Institute
Dana-Farber Cancer Institute
Hebrew University of Jerusalem

Research output: Contribution to journal › Article › peer-review

240 Citations (Scopus)

Abstract

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.

Original language	English
Article number	e17473
Journal	eLife
Volume	5
Issue number	NOVEMBER2016
DOIs	https://doi.org/10.7554/eLife.17473
Publication status	Published - Nov 18 2016
Externally published	Yes

Funding

We are grateful to all the members of the Kolter lab for valuable discussions and assistance. We are thankful to Dr. William Balch and David Drapeau (Bigelow Laboratory for Ocean Sciences, East Boothbay, ME) for their invaluable assistance in obtaining environmental samples. We thank Dr. Mor Grinstein and Dr. Jenna Galloway (Harvard Stem Cell Institute, Massachusetts General Hospital and Harvard Medical School, Boston, MA) for their generous help with the TUNEL assay. We thank Keith Ketterer from the Information Technology department at Harvard Medical School for help with video acquisition. We thank the Harvard Center for Nanoscale Systems for use of its imaging facility. This study was supported by fellowships from the European Molecular Biology Organization and from the Human Frontier Science Program granted to ES, DFG Transregio TRR-51 Roseobacter granted to JP, PCMM grant and NIH grant S10 RR023459 to NB., NIH grant GM086258 to JC and NIH grants GM58213 and GM82137 to RK. European Molecular Biology Organization LTF 649-2012 Einat Segev Human Frontier Science Program LT000061/2013-L Einat Segev Deutsche Forschungsgemeinschaft Transregio TRR-51 Roseobacter J?rn Petersen Program in Cellular and Molecular Medicine, Boston Children?s Hospital Natasha Barteneva National Institutes of Health RR023459 Natasha Barteneva National Institutes of Health GM086258 Jon Clardy National Institutes of Health GM58213 Roberto Kolter National Institutes of Health GM82137 Roberto Kolter The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

ASJC Scopus subject areas

General Neuroscience
General Biochemistry,Genetics and Molecular Biology
General Immunology and Microbiology

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10.7554/eLife.17473

Cite this

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title = "Dynamic metabolic exchange governs a marine algal-bacterial interaction",

abstract = "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.",

author = "Einat Segev and Wyche, \{Thomas P.\} and Kim, \{Ki Hyun\} and J{\"o}rn Petersen and Claire Ellebrandt and Hera Vlamakis and Natasha Barteneva and Paulson, \{Joseph N.\} and Liraz Chai and Jon Clardy and Roberto Kolter",

note = "Funding Information: We are grateful to all the members of the Kolter lab for valuable discussions and assistance. We are thankful to Dr. William Balch and David Drapeau (Bigelow Laboratory for Ocean Sciences, East Boothbay, ME) for their invaluable assistance in obtaining environmental samples. We thank Dr. Mor Grinstein and Dr. Jenna Galloway (Harvard Stem Cell Institute, Massachusetts General Hospital and Harvard Medical School, Boston, MA) for their generous help with the TUNEL assay. We thank Keith Ketterer from the Information Technology department at Harvard Medical School for help with video acquisition. We thank the Harvard Center for Nanoscale Systems for use of its imaging facility. This study was supported by fellowships from the European Molecular Biology Organization and from the Human Frontier Science Program granted to ES, DFG Transregio TRR-51 Roseobacter granted to JP, PCMM grant and NIH grant S10 RR023459 to NB., NIH grant GM086258 to JC and NIH grants GM58213 and GM82137 to RK. European Molecular Biology Organization LTF 649-2012 Einat Segev Human Frontier Science Program LT000061/2013-L Einat Segev Deutsche Forschungsgemeinschaft Transregio TRR-51 Roseobacter J?rn Petersen Program in Cellular and Molecular Medicine, Boston Children?s Hospital Natasha Barteneva National Institutes of Health RR023459 Natasha Barteneva National Institutes of Health GM086258 Jon Clardy National Institutes of Health GM58213 Roberto Kolter National Institutes of Health GM82137 Roberto Kolter The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} Segev et al.",

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doi = "10.7554/eLife.17473",

language = "English",

volume = "5",

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T1 - Dynamic metabolic exchange governs a marine algal-bacterial interaction

AU - Segev, Einat

AU - Wyche, Thomas P.

AU - Kim, Ki Hyun

AU - Petersen, Jörn

AU - Ellebrandt, Claire

AU - Vlamakis, Hera

AU - Barteneva, Natasha

AU - Paulson, Joseph N.

AU - Chai, Liraz

AU - Clardy, Jon

AU - Kolter, Roberto

N1 - Funding Information: We are grateful to all the members of the Kolter lab for valuable discussions and assistance. We are thankful to Dr. William Balch and David Drapeau (Bigelow Laboratory for Ocean Sciences, East Boothbay, ME) for their invaluable assistance in obtaining environmental samples. We thank Dr. Mor Grinstein and Dr. Jenna Galloway (Harvard Stem Cell Institute, Massachusetts General Hospital and Harvard Medical School, Boston, MA) for their generous help with the TUNEL assay. We thank Keith Ketterer from the Information Technology department at Harvard Medical School for help with video acquisition. We thank the Harvard Center for Nanoscale Systems for use of its imaging facility. This study was supported by fellowships from the European Molecular Biology Organization and from the Human Frontier Science Program granted to ES, DFG Transregio TRR-51 Roseobacter granted to JP, PCMM grant and NIH grant S10 RR023459 to NB., NIH grant GM086258 to JC and NIH grants GM58213 and GM82137 to RK. European Molecular Biology Organization LTF 649-2012 Einat Segev Human Frontier Science Program LT000061/2013-L Einat Segev Deutsche Forschungsgemeinschaft Transregio TRR-51 Roseobacter J?rn Petersen Program in Cellular and Molecular Medicine, Boston Children?s Hospital Natasha Barteneva National Institutes of Health RR023459 Natasha Barteneva National Institutes of Health GM086258 Jon Clardy National Institutes of Health GM58213 Roberto Kolter National Institutes of Health GM82137 Roberto Kolter The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: © Segev et al.

PY - 2016/11/18

Y1 - 2016/11/18

N2 - 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.

AB - 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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DO - 10.7554/eLife.17473

M3 - Article

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AN - SCOPUS:85006060222

SN - 2050-084X

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JO - eLife

JF - eLife

IS - NOVEMBER2016

M1 - e17473

ER -

Dynamic metabolic exchange governs a marine algal-bacterial interaction

Abstract

Funding

UN SDGs

ASJC Scopus subject areas

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