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

Abstract

Vestimentiferan tubeworms are iconic animals that present as large habitat-forming chitinised tube bushes in deep-sea chemosynthetic ecosystems. They are gutless and depend entirely on their endosymbiotic sulphide-oxidising 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 remodelled 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.

Novel Insights on Obligate Symbiont Lifestyle and Adaptation to Chemosynthetic Environment as Revealed by the Giant Tubeworm Genome

“…Hox7 , lox 2, and lox5 are missing from Lamellibrachia genome suggesting a possible loss of the central Hox cluster elements ( fig. 2 B ), contradicting recent results ( Sun et al 2021 ) (but see supplementary note 2 , Supplementary Material online ). The Hox-like elements, homeotic genes equally important for body plan specification and developmental processes, gbx , evx , mox , mnx , en , and dlx were also found in the giant tubeworm genome.…”

“…8 and 9 and supplementary note 2 , Supplementary Material online ). The same complement and synteny were identified in the chromosomal-level genome of Paraescarpia ( Sun et al 2021 ), attesting the good completeness and contiguity of the Riftia genome. We did not identify hox7 in Riftia , indicating a secondary loss of this gene in the giant tubeworm, a pattern also observed in other lophotrochozoan representatives such as phoronids ( Luo et al 2018 ) and bivalves ( Gerdol et al 2015 ; Calcino et al 2019 ).…”

“…21–24 , and supplementary tables 5 and 6 , Supplementary Material online ). Additionally, integrated genomic, transcriptomic, and proteomic analyses in Paraescarpia revealed a fairly similar scenario ( Sun et al 2021 ), pointing to common and shared molecular mechanisms involved with tube formation in cold-seep and vent vestimentiferans.…”

“…The BUSCO4 ( Simão et al 2015 ) genome completeness score is 99.37%. These numbers render Riftia the most complete annelid genome to date ( Simakov et al 2013 ; Li et al 2019 ; Martín-Durán et al 2020 ; Sun et al 2021 ) ( supplementary fig. 6 , Supplementary Material online ).…”

“…By analyzing the genome and transcriptomes of Riftia in a comparative framework, we highlight many evolutionary adaptations related to the obligate symbiotic lifestyle and survival in the deep-sea hydrothermal vent environment. The Riftia genome, together with a transcriptome and proteome study ( Hinzke et al 2019 ), a transcriptome study on the close relative Ridgeia piscesae ( Nyholm et al 2012 ), the genomic resources available for other close related tubeworms ( L. luymesi —short Lamellibrachia ; Paraescarpia echinospica —short Paraescarpia ) ( Li et al 2019 ; Sun et al 2021 ), and an extensive body of research broadens our understanding of one of the most conspicuous models for host–symbiont interaction and of the biology of Vestimentifera. Most importantly, we show that the developmental gene repertoire is conserved, and that besides the well-known nutritional aspect of the trophosome, its mesodermal origin brought an inherited suite of functions such as, hematopoiesis, endosomal digestion of endosymbionts, and storage of excretory products likely adapted to serve host–symbiont physiological interactions.…”