Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis

Yi Lan, Jin Sun, Chong Chen, Yanan Sun, Yadong Zhou, Yi Yang, Weipeng Zhang, Runsheng Li, Kun Zhou, Wai Chuen Wong, Yick Hang Kwan, Aifang Cheng, Salim Bougouffa, Cindy Lee Van Dover, Jian-Wen Qiu and Pei-Yuan Qian ()
Additional contact information
Yi Lan: The Hong Kong University of Science and Technology
Jin Sun: The Hong Kong University of Science and Technology
Chong Chen: X-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC)
Yanan Sun: The Hong Kong University of Science and Technology
Yadong Zhou: Second Institute of Oceanography, Ministry of Natural Resources
Yi Yang: The Hong Kong University of Science and Technology
Weipeng Zhang: Ocean University of China
Runsheng Li: City University of Hong Kong
Kun Zhou: The Hong Kong University of Science and Technology
Wai Chuen Wong: The Hong Kong University of Science and Technology
Yick Hang Kwan: The Hong Kong University of Science and Technology
Aifang Cheng: The Hong Kong University of Science and Technology
Salim Bougouffa: King Abdullah University of Science and Technology
Cindy Lee Van Dover: Duke University
Jian-Wen Qiu: Hong Kong Baptist University
Pei-Yuan Qian: The Hong Kong University of Science and Technology

Nature Communications, 2021, vol. 12, issue 1, 1-15

Abstract: Abstract Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.

Date: 2021
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DOI: 10.1038/s41467-021-21450-7

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