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, Pei-Yuan Qian

    Research output: Contribution to journalArticlepeer-review

    45 Scopus citations

    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.
    Original languageEnglish (US)
    JournalNature communications
    Volume12
    Issue number1
    DOIs
    StatePublished - Feb 20 2021

    Bibliographical note

    KAUST Repository Item: Exported on 2021-02-23
    Acknowledgements: We thank the captain and crew of the R/V Xiangyanghong 9 and pilots of HOV Jiaolong for their great support during the research cruise DY35th-II, the captain and crew of the R/V Dayang Yihao as well as the operation team of the ROV Sea Dragon III during the third leg of the China Ocean Mineral Resources Research and Development Association DY52nd cruise. Dr. Jack C.H. Ip and Dr. Ting Xu from Hong Kong Baptist University, as well as Dr. Ken Takai and Dr. Shinsuke Kawagucci from JAMSTEC are gratefully acknowledged for their helpful comments. Katsuyuki Uematsu (Marine Works Japan Ltd.) is thanked for his help during the TEM observations. This work was supported by grants from the National Key R&D Program of China (2018YFC0309904), China Ocean Mineral Resources Research and Development Association (DY135-E2-1-03), the Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (SMSEGL20SC01), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0409), and Major Project of Basic and Applied Basic Research of Guangdong Province (2019B030302004-04).

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