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

Yi Lan,Wai Chuen Wong,Jian-Wen Qiu,Yi Yang,Runsheng Li,Kun Zhou,Cindy Lee Van Dover,Yadong Zhou,Pei-Yuan Qian,Jin Sun,Yanan Sun,Aifang Cheng,Chong Chen,Weipeng Zhang,Salim Bougouffa,Yick Hang Kwan

doi:10.1038/s41467-021-21450-7

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.

Highlights

Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions
The endosymbionts housed in internal organs without direct contact with the vent fluid are likely to be reliant on the host for transporting substances such as oxygen, sulfide, and methane; diffusion may play a role in their delivery to the symbionts
The anatomical organisation of the endosymbionts in these two peltospirid snails are more similar to tubeworms than other known molluscan symbioses in vents[14,18] and the endosymbionts housed in the internal trophosome of the giant tubeworm R. pachyptila rely on the host’s haemoglobins to transport oxygen and sulfide[19]

Summary

Introduction

Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. A total of 21,438 genes (Supplementary Data 1) were predicted from the G. aegis genome, of which 1782 genes were highly expressed in the symbiont-hosting oesophageal gland (Supplementary Data 2).

Results

Conclusion