Genomic Signatures Supporting the Symbiosis and Formation of Chitinous Tube in the Deep-Sea Tubeworm Paraescarpia echinospica

Yanan SUN, Jin Sun, Yi Yang, Yi Lan, Chi Ho IP, Wai Chuen Wong, Yick Hang Kwan, Yanjie ZHANG, Zhuang Han, Jianwen QIU*, Pei Yuan Qian*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Vestimentiferan tubeworms are iconic animals that present as large habitat-forming chitinized tube bushes in deep-sea chemosynthetic ecosystems. They are gutless and depend entirely on their endosymbiotic sulfide-oxidizing chemoautotrophic bacteria for nutrition. Information on the genomes of several siboglinid endosymbionts has improved our understanding of their nutritional supplies. However, the interactions between tubeworms and their endosymbionts remain largely unclear due to a paucity of host genomes. Here, we report the chromosome-level genome of the vestimentiferan tubeworm Paraescarpia echinospica. We found that the genome has been remodeled to facilitate symbiosis through the expansion of gene families related to substrate transfer and innate immunity, suppression of apoptosis, regulation of lysosomal digestion, and protection against oxidative stress. Furthermore, the genome encodes a programmed cell death pathway that potentially controls the endosymbiont population. Our integrated genomic, transcriptomic, and proteomic analyses uncovered matrix proteins required for the formation of the chitinous tube and revealed gene family expansion and co-option as evolutionary mechanisms driving the acquisition of this unique supporting structure for deep-sea tubeworms. Overall, our study provides novel insights into the host’s support system that has enabled tubeworms to establish symbiosis, thrive in deep-sea hot vents and cold seeps, and produce the unique chitinous tubes in the deep sea.
Original languageEnglish
Pages (from-to)4116–4134
Number of pages19
JournalMolecular Biology and Evolution
Volume38
Issue number10
Early online date13 Jul 2021
DOIs
Publication statusPublished - Oct 2021

User-Defined Keywords

  • vestimentiferan
  • chemosynthetic symbiosis
  • comparative genomics
  • chitinous tube

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