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

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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.

Data availability

Microarray information and the data series are accessible at NCBI GEO under accession number GPL23280 and GSE97633 respectively. All the results of microarray analysis are included in Supplementary Table 1.The Whole Genome Shotgun project of Chlorella sp. A99 has been deposited at DDBJ/ENA/GenBank under the accession PCFQ00000000 (BioProject ID: PRJNA412448). Genome sequences and gene models are also accessible at the website of OIST Marine Genomics Unit Genome Project (http://marinegenomics.oist.jp/chlorellaA99/viewer/info?project_id=65).All data generated by qPCR are included in Source Data: Figure2, Figure2 - Figure supplement 1, Source Data: Figure3, Source Data: Figure3 - Figure Supplement 2 and Source Data: Table 2, Table 4

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Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0001-7306-2032
Katja Schröder

Zoological Institute, Kiel University, Kiel, Germany

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The authors declare that no competing interests exist.
Jay Bathia

Zoological Institute, Kiel University, Kiel, Germany

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The authors declare that no competing interests exist.
Ulrich Kürn

Zoological Institute, Kiel University, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.
Sebastian Fraune

Zoological Institute, Kiel University, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6940-9571
Mariia Khalturina

Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan

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The authors declare that no competing interests exist.
Konstantin Khalturin

Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4359-2993
Chuya Shinzato

Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7843-3381
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.

"This ORCID iD identifies the author of this article:" 0000-0002-4480-3572
Thomas C G Bosch

Zoological Institute, Kiel University, Kiel, Germany

For correspondence
tbosch@zoologie.uni-kiel.de

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The authors declare that no competing interests exist.

"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.

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