Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms

Giacomo Moggioli, Balig Panossian, Yanan Sun, Daniel Thiel, Francisco M. Martín-Zamora, Martin Tran, Alexander M. Clifford, Shana K. Goffredi, Nadezhda Rimskaya-Korsakova, Gáspár Jékely, Martin Tresguerres, Pei-Yuan Qian, Jian-Wen Qiu, Greg W. Rouse, Lee M. Henry () and José M. Martín-Durán ()
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Giacomo Moggioli: Queen Mary University of London
Balig Panossian: Queen Mary University of London
Yanan Sun: The Hong Kong University of Science and Technology
Daniel Thiel: University of Exeter
Francisco M. Martín-Zamora: Queen Mary University of London
Martin Tran: Queen Mary University of London
Alexander M. Clifford: University of California, San Diego
Shana K. Goffredi: Occidental College
Nadezhda Rimskaya-Korsakova: Friedrich Schiller University Jena, Faculty of Biological Sciences, Institute of Zoology and Evolutionary Research
Gáspár Jékely: University of Exeter
Martin Tresguerres: University of California, San Diego
Pei-Yuan Qian: The Hong Kong University of Science and Technology
Jian-Wen Qiu: Hong Kong Baptist University
Greg W. Rouse: University of California, San Diego
Lee M. Henry: Queen Mary University of London
José M. Martín-Durán: Queen Mary University of London

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbioses remain unclear. Here, we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. Genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi from the chemoautotrophic symbiosis of deep-sea Vestimentifera. Osedax’s endosymbionts complement many of the host’s metabolic deficiencies, including the loss of pathways to recycle nitrogen and synthesise some amino acids. Osedax’s endosymbionts possess the glyoxylate cycle, which could allow more efficient catabolism of bone-derived nutrients and the production of carbohydrates from fatty acids. Unlike in most Vestimentifera, innate immunity genes are reduced in O. frankpressi, which, however, has an expansion of matrix metalloproteases to digest collagen. Our study supports that distinct nutritional interactions influence host genome evolution differently in highly specialised symbioses.

Date: 2023
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Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38521-6

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DOI: 10.1038/s41467-023-38521-6

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