Genomic adaptations to chemosymbiosis in the deep-sea seep-dwelling tubeworm Lamellibrachia luymesi

Abstract

BackgroundSymbiotic relationships between microbes and their hosts are widespread and diverse, often providing protection or nutrients, and may be either obligate or facultative. However, the genetic mechanisms allowing organisms to maintain host-symbiont associations at the molecular level are still mostly unknown, and in the case of bacterial-animal associations, most genetic studies have focused on adaptations and mechanisms of the bacterial partner. The gutless tubeworms (Siboglinidae, Annelida) are obligate hosts of chemoautotrophic endosymbionts (except for Osedax which houses heterotrophic Oceanospirillales), which rely on the sulfide-oxidizing symbionts for nutrition and growth. Whereas several siboglinid endosymbiont genomes have been characterized, genomes of hosts and their adaptations to this symbiosis remain unexplored.ResultsHere, we present and characterize adaptations of the cold seep-dwelling tubeworm Lamellibrachia luymesi, one of the longest-lived solitary invertebrates. We sequenced the worm’s ~ 688-Mb haploid genome with an overall completeness of ~ 95% and discovered that L. luymesi lacks many genes essential in amino acid biosynthesis, obligating them to products provided by symbionts. Interestingly, the host is known to carry hydrogen sulfide to thiotrophic endosymbionts using hemoglobin. We also found an expansion of hemoglobin B1 genes, many of which possess a free cysteine residue which is hypothesized to function in sulfide binding. Contrary to previous analyses, the sulfide binding mediated by zinc ions is not conserved across tubeworms. Thus, the sulfide-binding mechanisms in sibgolinids need to be further explored, and B1 globins might play a more important role than previously thought. Our comparative analyses also suggest the Toll-like receptor pathway may be essential for tolerance/sensitivity to symbionts and pathogens. Several genes related to the worm’s unique life history which are known to play important roles in apoptosis, cell proliferation, and aging were also identified. Last, molecular clock analyses based on phylogenomic data suggest modern siboglinid diversity originated in 267 mya (± 70 my) support previous hypotheses indicating a Late Mesozoic or Cenozoic origins of approximately 50–126 mya for vestimentiferans.ConclusionsHere, we elucidate several specific adaptations along various molecular pathways that link phenome to genome to improve understanding of holobiont evolution. Our findings of adaptation in genomic mechanisms to reducing environments likely extend to other chemosynthetic symbiotic systems.

Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis

“…7 ). The TLR proteins serve as key molecular linkages between the host and bacteria in bacterial invasion and host recognition, and they are expanded in the deep-sea tubeworm Lamellibrachia luymesi 37 . These observations indicate that TLR proteins play an important role in symbiosis establishment across different deep-sea animals.…”

Contrasting influences on bacterial symbiont specificity by co‐occurring deep‐sea mussels and tubeworms

“…Previous observations of tubeworms at other hydrothermal vent and seep sites suggest the lack of influence of local sampling sites or host species on symbiont composition in co-occurring vestimentiferan tubeworms (McMullin et al, 2003;Zimmermann et al, 2014;Reveillaud et al, 2018). With regard to their selection of a particular symbiont from the environment, Li et al (2019) have identified a number of toll-like receptors, and other genes (NLRP gene family) in the genome of Lamellibrachia luymesi speculated to be involved in the innate immune recognition of infectious pathogens or symbionts. Additionally, comparative genomic studies of the chemoautotrophic symbionts of Escarpia and Lamellibrachia from the Gulf of Mexico, and Riftia pachyptila from the East Pacific Rise, revealed several adhesion-related proteins in the symbiont genomes, including a fibronectin type III domain, so far only found to date in vent-dwelling vestimentiferan symbionts and thought to be involved in initial attachment to the host surface (Gardebrecht et al, 2012;Li et al, 2018).…”

Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome

“…CC-BY-NC-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted September 6, 2021. ; https://doi.org/10.1101/2021.09.04.458960 doi: bioRxiv preprint Overall, endosomal-associated digestion of endosymbionts seems to be a hallmark of intracellular digestion accomplished in the mesodermal trophosome of vestimentiferans, such as Riftia and Lamellibrachia (Nussbaumer et al 2006;Hinzke et al 2019;Li et al 2019) (see also below). This process serves the host nutrition as well as the control of the symbiont population density during host growth, known from many other symbioses (Angela E. Douglas 2010).…”

“…By analysing 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 another close relative Lamellibrachia luymesi (Li et al 2019) (short Lamellibrachia), and an extensive body of research . CC-BY-NC-ND 4.0 International license perpetuity.…”