1. Evolutionary Biology
Download icon

Metabolic co-dependence drives the evolutionarily ancient Hydra-Chlorella symbiosis

  1. Mayuko Hamada
  2. Katja Schröder
  3. Jay Bathia
  4. Ulrich Kürn
  5. Sebastian Fraune
  6. Mariia Khalturina
  7. Konstantin Khalturin
  8. Chuya Shinzato
  9. Nori Satoh
  10. Thomas C G Bosch  Is a corresponding author
  1. Okinawa Institute of Science and Technology Graduate University (OIST), Japan
  2. Kiel University, Germany
Research Article
  • Cited 15
  • Views 3,692
  • Annotations
Cite this article as: eLife 2018;7:e35122 doi: 10.7554/eLife.35122

Abstract

Many multicellular organisms rely on symbiotic associations for support of metabolic activity, protection, or energy. Understanding the mechanisms involved in controlling such interactions remains a major challenge. In an unbiased approach we identified key players that control the symbiosis between Hydra viridissima and its photosynthetic symbiont Chlorella sp. A99. We discovered significant up-regulation of Hydra genes encoding a phosphate transporter and glutamine synthetase suggesting regulated nutrition supply between host and symbionts. Interestingly, supplementing the medium with glutamine temporarily supports in vitro growth of the otherwise obligate symbiotic Chlorella, indicating loss of autonomy and dependence on the host. Genome sequencing of Chlorella sp. A99 revealed a large number of amino acid transporters and a degenerated nitrate assimilation pathway, presumably as consequence of the adaptation to the host environment. Our observations portray ancient symbiotic interactions as a codependent partnership in which exchange of nutrients appears to be the primary driving force.

Article and author information

Author details

  1. Mayuko Hamada

    Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7306-2032

  2. Katja Schröder

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Jay Bathia

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Ulrich Kürn

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Sebastian Fraune

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6940-9571

  6. Mariia Khalturina

    Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.

  7. Konstantin Khalturin

    Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4359-2993

  8. Chuya Shinzato

    Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7843-3381

  9. Nori Satoh

    Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4480-3572

  10. Thomas C G Bosch

    Zoological Institute, Kiel University, Kiel, Germany
    For correspondence
    tbosch@zoologie.uni-kiel.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9488-5545

Funding

Japan Society for the Promotion of Science (Young Scientists (B) 25840132)

  • Mayuko Hamada

Japan Society for the Promotion of Science (Scientific Research (C) 15K07173)

  • Mayuko Hamada

Deutsche Forschungsgemeinschaft (CRC1182)

  • Thomas C G Bosch

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: January 16, 2018
  2. Accepted: May 26, 2018
  3. Accepted Manuscript published: May 31, 2018 (version 1)
  4. Version of Record published: June 26, 2018 (version 2)

Copyright

© 2018, Hamada 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

  • 3,692
    Page views
  • 395
    Downloads
  • 15
    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)

Categories and tags

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics

    Rapid adaptation to malaria facilitated by admixture in the human population of Cabo Verde

    Iman Hamid et al.
    Research Article Updated

    Humans have undergone large migrations over the past hundreds to thousands of years, exposing ourselves to new environments and selective pressures. Yet, evidence of ongoing or recent selection in humans is difficult to detect. Many of these migrations also resulted in gene flow between previously separated populations. These recently admixed populations provide unique opportunities to study rapid evolution in humans. Developing methods based on distributions of local ancestry, we demonstrate that this sort of genetic exchange has facilitated detectable adaptation to a malaria parasite in the admixed population of Cabo Verde within the last ~20 generations. We estimate that the selection coefficient is approximately 0.08, one of the highest inferred in humans. Notably, we show that this strong selection at a single locus has likely affected patterns of ancestry genome-wide, potentially biasing demographic inference. Our study provides evidence of adaptation in a human population on historical timescales.

    1. Evolutionary Biology

    Evidence for adaptive evolution in the receptor-binding domain of seasonal coronaviruses OC43 and 229E

    Kathryn E Kistler, Trevor Bedford
    Research Article

    Seasonal coronaviruses (OC43, 229E, NL63 and HKU1) are endemic to the human population, regularly infecting and reinfecting humans while typically causing asymptomatic to mild respiratory infections. It is not known to what extent reinfection by these viruses is due to waning immune memory or antigenic drift of the viruses. Here, we address the influence of antigenic drift on immune evasion of seasonal coronaviruses. We provide evidence that at least two of these viruses, OC43 and 229E, are undergoing adaptive evolution in regions of the viral spike protein that are exposed to human humoral immunity. This suggests that reinfection may be due, in part, to positively-selected genetic changes in these viruses that enable them to escape recognition by the immune system. It is possible that, as with seasonal influenza, these adaptive changes in antigenic regions of the virus would necessitate continual reformulation of a vaccine made against them.

    1. Evolutionary Biology

    Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations

    Milo S Johnson et al.
    Research Article

    Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 Saccharomyces cerevisiae populations (124 haploid and 81 diploid) for ~10,000,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in E. coli, we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions.