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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 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.

SUBMITTER: Sun Y

PROVIDER: S-EPMC8476170 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Symbiotic 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. RESULTS:Here, 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. CONCLUSIONS:Here, 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.

Project description:Use of hydrogen gas (H2) as an electron donor is common among free-living chemolithotrophic microorganisms. Given the presence of this dissolved gas at deep-sea hydrothermal vents, it has been suggested that it may also be a major electron donor for the free-living and symbiotic chemolithoautotrophic bacteria that are the primary producers at these sites. Giant Riftia pachyptila siboglinid tubeworms and their symbiotic bacteria ("Candidatus Endoriftia persephone") dominate many vents in the Eastern Pacific, and their use of sulfide as a major electron donor has been documented. Genes encoding hydrogenase are present in the "Ca Endoriftia persephone" genome, and proteome data suggest that these genes are expressed. In this study, high-pressure respirometry of intact R. pachyptila and incubations of trophosome homogenate were used to determine whether this symbiotic association could also use H2 as a major electron donor. Measured rates of H2 uptake by intact R. pachyptila in high-pressure respirometers were similar to rates measured in the absence of tubeworms. Oxygen uptake rates in the presence of H2 were always markedly lower than those measured in the presence of sulfide, as was the incorporation of 13C-labeled dissolved inorganic carbon. Carbon fixation by trophosome homogenate was not stimulated by H2, nor was hydrogenase activity detectable in these samples. Though genes encoding [NiFe] group 1e and [NiFe] group 3b hydrogenases are present in the genome and transcribed, it does not appear that H2 is a major electron donor for this system, and it may instead play a role in intracellular redox homeostasis.IMPORTANCE Despite the presence of hydrogenase genes, transcripts, and proteins in the "Ca Endoriftia persephone" genome, transcriptome, and proteome, it does not appear that R. pachyptila can use H2 as a major electron donor. For many uncultivable microorganisms, omic analyses are the basis for inferences about their activities in situ However, as is apparent from the study reported here, there are dangers in extrapolating from omics data to function, and it is essential, whenever possible, to verify functions predicted from omics data with physiological and biochemical measurements.

Project description:BackgroundLamellibrachia luymesi dominates cold sulfide-hydrocarbon seeps and is known for its ability to consume bacteria for energy. The symbiotic relationship between tubeworms and bacteria with particular adaptations to chemosynthetic environments has received attention. However, metabolic studies have primarily focused on the mechanisms and pathways of the bacterial symbionts, while studies on the animal hosts are limited.ResultsHere, we sequenced the transcriptome of L. luymesi and generated a transcriptomic database containing 79,464 transcript sequences. Based on GO and KEGG annotations, we identified transcripts related to sulfur metabolism, sterol biosynthesis, trehalose synthesis, and hydrolysis. Our in-depth analysis identified sulfation pathways in L. luymesi, and sulfate activation might be an important detoxification pathway for promoting sulfur cycling, reducing byproducts of sulfide metabolism, and converting sulfur compounds to sulfur-containing organics, which are essential for symbiotic survival. Moreover, sulfide can serve directly as a sulfur source for cysteine synthesis in L. luymesi. The existence of two pathways for cysteine synthesis might ensure its participation in the formation of proteins, heavy metal detoxification, and the sulfide-binding function of haemoglobin. Furthermore, our data suggested that cold-seep tubeworm is capable of de novo sterol biosynthesis, as well as incorporation and transformation of cycloartenol and lanosterol into unconventional sterols, and the critical enzyme involved in this process might have properties similar to those in the enzymes from plants or fungi. Finally, trehalose synthesis in L. luymesi occurs via the trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) pathways. The TPP gene has not been identified, whereas the TPS gene encodes a protein harbouring conserved TPS/OtsA and TPP/OtsB domains. The presence of multiple trehalases that catalyse trehalose hydrolysis could indicate the different roles of trehalase in cold-seep tubeworms.ConclusionsWe elucidated several molecular pathways of sulfate activation, cysteine and cholesterol synthesis, and trehalose metabolism. Contrary to the previous analysis, two pathways for cysteine synthesis and the cycloartenol-C-24-methyltransferase gene were identified in animals for the first time. The present study provides new insights into particular adaptations to chemosynthetic environments in L. luymesi and can serve as the basis for future molecular studies on host-symbiont interactions and biological evolution.

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

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