Endosymbiont population genomics sheds light on transmission mode, partner specificity, and stability of the scaly-foot snail holobiont

Yi Lan, Jin Sun, Chong Chen, Hao Wang, Yao Xiao, Maeva Perez, Yi Yang, Yick Hang Kwan, Yanan Sun, Yadong Zhou, Xiqiu Han, Junichi Miyazaki, Tomo O Watsuji, Dass Bissessur, Jian Wen Qiu, Ken Takai, Pei Yuan Qian*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host’s cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.

Original languageEnglish
Pages (from-to)2132-2143
Number of pages12
JournalISME Journal
Volume16
Issue number9
Early online date17 Jun 2022
DOIs
Publication statusPublished - Sep 2022

Scopus Subject Areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

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