Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria : Insights from multi-omics analysis

Yi-Tao LIN, Ting XU, Jack Chi-Ho IP, Yanan SUN, Ling FANG, Tiangang LUAN, Yu ZHANG*, Pei-Yuan QIAN*, Jian-Wen QIU*

*Corresponding author for this work

Research output: Journal PublicationsJournal Article (refereed)peer-review

5 Citations (Scopus)

Abstract

Endosymbiosis with Gammaproteobacteria is fundamental for the success of bathymodioline mussels in deep-sea chemosynthesis-based ecosystems. However, the recent discovery of Campylobacteria on the gill surfaces of these mussels suggests that these host-bacterial relationships may be more complex than previously thought. Using the cold-seep mussel (Gigantidas haimaensis) as a model, we explored this host-bacterial system by assembling the host transcriptome and genomes of its epibiotic Campylobacteria and endosymbiotic Gammaproteobacteria and quantifying their gene and protein expression levels. We found that the epibiont applies a sulfur oxidizing (SOX) multienzyme complex with the acquisition of soxB from Gammaproteobacteria for energy production and switched from a reductive tricarboxylic acid (rTCA) cycle to a Calvin-Benson-Bassham (CBB) cycle for carbon assimilation. The host provides metabolic intermediates, inorganic carbon, and thiosulfate to satisfy the materials and energy requirements of the epibiont, but whether the epibiont benefits the host is unclear. The endosymbiont adopts methane oxidation and the ribulose monophosphate pathway (RuMP) for energy production, providing the major source of energy for itself and the host. The host obtains most of its nutrients, such as lysine, glutamine, valine, isoleucine, leucine, histidine, and folate, from the endosymbiont. In addition, host pattern recognition receptors, including toll-like receptors, peptidoglycan recognition proteins, and C-type lectins, may participate in bacterial infection, maintenance, and population regulation. Overall, this study provides insights into the complex host-bacterial relationships that have enabled mussels and bacteria to thrive in deep-sea chemosynthetic ecosystems.

Original languageEnglish
Pages (from-to)106-125
Number of pages20
JournalZoological research
Volume44
Issue number1
DOIs
Publication statusPublished - Jan 2023
Externally publishedYes

Bibliographical note

Funding Information:
This study was supported by the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0409, SMSEGL20SC02), Research Grants Council of Hong Kong (12101021), and Guangdong Natural Science Foundation (2020A1515011117)

Publisher Copyright:
Copyright © 2023 Editorial Office of Zoological Research, Kunming Institute of Zoology, Chinese Academy of Sciences.

Keywords

  • Bathymodioline
  • Chemosynthesis
  • Cold seep
  • Deep-sea adaptation
  • Symbiosis

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