Host-Endosymbiont Genome Integration in a Deep-Sea Chemosymbiotic Clam

Jack Chi Ho Ip, Ting Xu, Jin Sun, Runsheng LI, Chong Chen, Yi Lan, Zhuang Han, Haibin Zhang, Jiangong Wei, Hongbin Wang, Jun Tao, Zongwei Cai, Pei Yuan Qian, Jian Wen Qiu*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)

Abstract

Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host's high dependence on the symbiont for nutrition. Overall, the host-symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.

Original languageEnglish
Pages (from-to)502-518
Number of pages17
JournalMolecular Biology and Evolution
Volume38
Issue number2
DOIs
Publication statusPublished - 1 Feb 2021

Scopus Subject Areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

User-Defined Keywords

  • cold seep
  • genome assembly
  • genome erosion
  • hydrothermal vent
  • Mollusca
  • symbiosis

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