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

Abstract

The mutualism between the giant tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has been extensively researched over the past 40 years. However, the lack of the host whole genome information has impeded the full comprehension of the genotype/phenotype interface in Riftia. Here we described the high-quality draft genome of Riftia, its complete mitogenome, and tissue-specific transcriptomic data. The Riftia genome presents signs of reductive evolution, with gene family contractions exceeding expansions. Expanded gene families are related to sulphur metabolism, detoxification, anti-oxidative stress, oxygen transport, immune system, and lysosomal digestion, reflecting evolutionary adaptations to the vent environment and endosymbiosis. Despite the derived body plan, the developmental gene repertoire in the gutless tubeworm is extremely conserved with the presence of a near intact and complete Hox cluster. Gene expression analyses establishes that the trophosome is a multi-functional organ marked by intracellular digestion of endosymbionts, storage of excretory products and haematopoietic functions. Overall, the plume and gonad tissues both in contact to the environment harbour highly expressed genes involved with cell cycle, programmed cell death, and immunity indicating a high cell turnover and defence mechanisms against pathogens. We posit that the innate immune system plays a more prominent role into the establishment of the symbiosis during the infection in the larval stage, rather than maintaining the symbiostasis in the trophosome. This genome bridges four decades of physiological research in Riftia, whilst simultaneously provides new insights into the development, whole organism functions and evolution in the giant tubeworm.

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

“…We generated almost completely de-haploidised draft assemblies (Supplementary Figure 2A-D), which included the circularised endosymbiont genomes of O. frankpressi and Oasisia alvinae and several epibionts associated with O. frankpressi (Supplementary Figure 2H-J; Supplementary Table 2). Consistent with k-mer-based analyses (Supplementary Figure 2E-G), previously reported genome size estimation for Oasisia alvinae (31), and a recent genome assembly of R. pachyptila (10), the assembled genomes for O. frankpressi, Oasisia alvinae and R. pachyptila span 285 Mb, 808 Mb and 554 Mb after removal of bacterial contigs, respectively (Figure 2A; Supplementary Figure 2K). For Oasisia alvinae and R. pachyptila, the genome assembly shows high completeness (96.9% and 95.6% BUSCO presence, respectively; Supplementary Figure 2L; Supplementary Table 3), yet the assembly for O. frankpressi appeared to have a lower completeness (80.1% BUSCO presence; Supplementary Figure 2L).…”

“…Although the genome of O. frankpressi is ∼50–75% smaller than the sequenced genomes and estimated genome sizes of Vestimentifera (Figure 2A) ( 8–10, 31 ), the fraction of simple repeats and transposable elements in O. frankpressi (29.16%) is comparable to that of the vestimentiferan R. pachyptila (27.87%) and asymbiotic annelids with similar genome sizes, such as Capitella teleta (31%) (Figure 2B; Supplementary Figure 3A). Moreover, as in Vestimentifera, but unlike asymbiotic annelids with slow rates of molecular evolution such as Owenia fusiformis and C. teleta ( 33, 34 ), the repeat landscape in O. frankpressi shows signs of expansions (Supplementary Figure 3B).…”

“…In addition of lacking a gut, Siboglinidae also lacks eyes and any other sensory structure in their most anterior region, the prostomium ( 27, 53 ). Yet unlike other annelids with unusual body plans such as the leech H. robusta ( 34 ), the genomes of Vestimentifera contain a complete developmental toolkit ( 9, 10 ). To investigate genes involved in body patterning and organogenesis in the reduced gene set of O. frankpressi , we first focused on the repertoire of G protein-coupled receptors (GPCRs).…”

“…Siboglinid worms (Annelida) often dominate deep-sea chemosynthetic environments through symbioses with environmentally acquired bacteria (5,6) that adults harbour within a specialised organ called a trophosome (7). Despite their ecological importance, our understanding of the genetic traits that sustain symbioses in Siboglinidae is scarce and currently limited to Vestimentifera (8)(9)(10), one of the four main lineages in this annelid group (Figure 1A). Loss of genes involved in amino acid biosynthesis (8,10) and carbohydrate catabolism (9) together with expansions of genes involved in nutrient transport (8), gas exchange (8)(9)(10)(11)(12), innate immunity and lysosomal digestion (8)(9)(10)13) show a complex molecular interplay between Vestimentifera and their endosymbionts to fulfil their nutritional demands (14).…”

“…Despite their ecological importance, our understanding of the genetic traits that sustain symbioses in Siboglinidae is scarce and currently limited to Vestimentifera (8)(9)(10), one of the four main lineages in this annelid group (Figure 1A). Loss of genes involved in amino acid biosynthesis (8,10) and carbohydrate catabolism (9) together with expansions of genes involved in nutrient transport (8), gas exchange (8)(9)(10)(11)(12), innate immunity and lysosomal digestion (8)(9)(10)13) show a complex molecular interplay between Vestimentifera and their endosymbionts to fulfil their nutritional demands (14). Notably, many of these genetic changes are common to Vestimentifera dwelling in both methane seeps and hydrothermal vents, and also to other distantly related chemosymbiotic animals such as bivalves (15), gastropods (16), and the clitellate annelid Olavius algarvensis (17).…”