1. Ecology
Download icon

Dynamic metabolic exchange governs a marine algal-bacterial interaction

  1. Einat Segev  Is a corresponding author
  2. Thomas P Wyche
  3. Ki Hyun Kim
  4. Jörn Petersen
  5. Claire Ellebrandt
  6. Hera Vlamakis
  7. Natasha Barteneva
  8. Joseph N Paulson
  9. Liraz Chai
  10. Jon Clardy
  11. Roberto Kolter  Is a corresponding author
  1. Harvard Medical School, United States
  2. Sungkyunkwan University, United States
  3. Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Germany
  4. Broad Institute, United States
  5. Dana-Farber Cancer Institute, United States
  6. The Hebrew University of Jerusalem, Israel
Research Article
  • Cited 76
  • Views 4,787
  • Annotations
Cite this article as: eLife 2016;5:e17473 doi: 10.7554/eLife.17473

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.

Article and author information

Author details

  1. Einat Segev

    Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United States
    For correspondence
    Einat_Segev@hms.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2266-1219
  2. Thomas P Wyche

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  3. Ki Hyun Kim

    School of Pharmacy, Sungkyunkwan University, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5285-9138
  4. Jörn Petersen

    Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany
    Competing interests
    No competing interests declared.
  5. Claire Ellebrandt

    Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany
    Competing interests
    No competing interests declared.
  6. Hera Vlamakis

    Broad Institute, Boston, United States
    Competing interests
    No competing interests declared.
  7. Natasha Barteneva

    Program in Cellular and Molecular Medicine, Boston Children's Hospital, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  8. Joseph N Paulson

    Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, United States
    Competing interests
    No competing interests declared.
  9. Liraz Chai

    Institute of Chemistry, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    No competing interests declared.
  10. Jon Clardy

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    Competing interests
    Jon Clardy, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0213-8356
  11. Roberto Kolter

    Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United States
    For correspondence
    roberto_kolter@hms.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9548-1481

Funding

European Molecular Biology Organization (LTF 649-2012)

  • Einat Segev

Human Frontier Science Program (LT000061/2013-L)

  • Einat Segev

DFG Transregio TRR-51 Roseobacter

  • Jörn Petersen

PCMM

  • 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.

Reviewing Editor

  1. Paul G Falkowski, Rutgers University, United States

Publication history

  1. Received: May 6, 2016
  2. Accepted: November 16, 2016
  3. Accepted Manuscript published: November 18, 2016 (version 1)
  4. Version of Record published: December 9, 2016 (version 2)

Copyright

© 2016, Segev et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,787
    Page views
  • 1,179
    Downloads
  • 76
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Ecology
    Ben G Weinstein et al.
    Tools and Resources Updated

    Forests provide biodiversity, ecosystem, and economic services. Information on individual trees is important for understanding forest ecosystems but obtaining individual-level data at broad scales is challenging due to the costs and logistics of data collection. While advances in remote sensing techniques allow surveys of individual trees at unprecedented extents, there remain technical challenges in turning sensor data into tangible information. Using deep learning methods, we produced an open-source data set of individual-level crown estimates for 100 million trees at 37 sites across the United States surveyed by the National Ecological Observatory Network’s Airborne Observation Platform. Each canopy tree crown is represented by a rectangular bounding box and includes information on the height, crown area, and spatial location of the tree. These data have the potential to drive significant expansion of individual-level research on trees by facilitating both regional analyses and cross-region comparisons encompassing forest types from most of the United States.

    1. Ecology
    Chen Chen et al.
    Research Article

    Insect pests negatively affect crop quality and yield; identifying new methods to protect crops against insects therefore has important agricultural applications. Our analysis of transgenic Arabidopsis thaliana plants showed that overexpression of PENTACYCLIC TRITERPENE SYNTHASE 1 (PEN1), encoding the key biosynthetic enzyme for the natural plant product (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), led to significant resistance against a major insect pest, Plustella xylostella. DMNT treatment severely damaged the peritrophic matrix (PM), a physical barrier isolating food and pathogens from the midgut wall cells. DMNT repressed the expression of PxMucin in midgut cells and knocking down PxMucin resulted in PM rupture and P. xylostella death. A 16S RNA survey revealed that DMNT significantly disrupted midgut microbiota populations and that midgut microbes were essential for DMNT-induced killing. Therefore, we propose that the midgut microbiota assists DMNT in killing P. xylostella. These findings may provide a novel approach for plant protection against P. xylostella.