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Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome

View ORCID ProfileAndré Luiz de Oliveira, Jessica Mitchell, Peter Girguis, Monika Bright
doi: https://doi.org/10.1101/2021.09.04.458960
André Luiz de Oliveira
1Department of Functional and Evolutionary Ecology, University of Vienna, Austria
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  • For correspondence: andre.luiz.de.oliveira@univie.ac.at
Jessica Mitchell
2Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
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Peter Girguis
2Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
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Monika Bright
1Department of Functional and Evolutionary Ecology, University of Vienna, Austria
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Abstract

The mutualism between the giant tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has been extensively researched over the past 40 years. However, the lack of the host whole genome information has impeded the full comprehension of the genotype/phenotype interface in Riftia. Here we described the high-quality draft genome of Riftia, its complete mitogenome, and tissue-specific transcriptomic data. The Riftia genome presents signs of reductive evolution, with gene family contractions exceeding expansions. Expanded gene families are related to sulphur metabolism, detoxification, anti-oxidative stress, oxygen transport, immune system, and lysosomal digestion, reflecting evolutionary adaptations to the vent environment and endosymbiosis. Despite the derived body plan, the developmental gene repertoire in the gutless tubeworm is extremely conserved with the presence of a near intact and complete Hox cluster. Gene expression analyses establishes that the trophosome is a multi-functional organ marked by intracellular digestion of endosymbionts, storage of excretory products and haematopoietic functions. Overall, the plume and gonad tissues both in contact to the environment harbour highly expressed genes involved with cell cycle, programmed cell death, and immunity indicating a high cell turnover and defence mechanisms against pathogens. We posit that the innate immune system plays a more prominent role into the establishment of the symbiosis during the infection in the larval stage, rather than maintaining the symbiostasis in the trophosome. This genome bridges four decades of physiological research in Riftia, whilst simultaneously provides new insights into the development, whole organism functions and evolution in the giant tubeworm.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 06, 2021.
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Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome
André Luiz de Oliveira, Jessica Mitchell, Peter Girguis, Monika Bright
bioRxiv 2021.09.04.458960; doi: https://doi.org/10.1101/2021.09.04.458960
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Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome
André Luiz de Oliveira, Jessica Mitchell, Peter Girguis, Monika Bright
bioRxiv 2021.09.04.458960; doi: https://doi.org/10.1101/2021.09.04.458960

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