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Symbiont-driven sulfur crystal formation in a thiotrophic symbiosis from deep-sea hydrocarbon seeps.

ABSTRACT: The siboglinid tubeworm Sclerolinum contortum symbiosis inhabits sulfidic sediments at deep-sea hydrocarbon seeps in the Gulf of Mexico. A single symbiont phylotype in the symbiont-housing organ is inferred from phylogenetic analyses of the 16S ribosomal ribonucleic acid (16S rRNA) gene and fluorescent in situ hybridization. The phylotype we studied here, and a previous study from an arctic hydrocarbon seep population, reveal identical 16S rRNA symbiont gene sequences. While sulfide is apparently the energy source for the symbionts (and ultimately the gutless host), both partners also have to cope with its toxicity. This study demonstrates abundant large sulfur crystals restricted to the trophosome area. Based on Raman microspectroscopy and energy dispersive X-ray analysis, these crystals have the same S8 sulfur configuration as the recently described small sulfur vesicles formed in the symbionts. The crystals reside adjacent to the symbionts in the trophosome. This suggests that their formation is either extra- or intracellular in symbionts. We propose that formation of these crystals provides both energy-storage compounds for the symbionts and serves the symbiosis by removing excess toxic sulfide from host tissues. This symbiont-mediated sulfide detoxification may have been crucial for the establishment of thiotrophic symbiosis and continues to remain an important function of the symbionts.

SUBMITTER: Eichinger I

PROVIDER: S-EPMC4232855 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Symbiont-driven sulfur crystal formation in a thiotrophic symbiosis from deep-sea hydrocarbon seeps.

Eichinger Irmgard I Schmitz-Esser Stephan S Schmid Markus M Fisher Charles R CR Bright Monika M

Environmental microbiology reports 20140303 4

The siboglinid tubeworm Sclerolinum contortum symbiosis inhabits sulfidic sediments at deep-sea hydrocarbon seeps in the Gulf of Mexico. A single symbiont phylotype in the symbiont-housing organ is inferred from phylogenetic analyses of the 16S ribosomal ribonucleic acid (16S rRNA) gene and fluorescent in situ hybridization. The phylotype we studied here, and a previous study from an arctic hydrocarbon seep population, reveal identical 16S rRNA symbiont gene sequences. While sulfide is apparentl ...[more]

PMID: 24992535

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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.

Dataset Information

Symbiont-driven sulfur crystal formation in a thiotrophic symbiosis from deep-sea hydrocarbon seeps.

Publications

Symbiont-driven sulfur crystal formation in a thiotrophic symbiosis from deep-sea hydrocarbon seeps.

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