Dataset Information

Chemosynthetic ectosymbionts associated with a shallow-water marine nematode.

ABSTRACT: Prokaryotes and free-living nematodes are both very abundant and co-occur in marine environments, but little is known about their possible association. Our objective was to characterize the microbiome of a neglected but ecologically important group of free-living benthic nematodes of the Oncholaimidae family. We used a multi-approach study based on microscopic observations (Scanning Electron Microscopy and Fluorescence In Situ Hybridization) coupled with an assessment of molecular diversity using metabarcoding based on the 16S rRNA gene. All investigated free-living marine nematode specimens harboured distinct microbial communities (from the surrounding water and sediment and through the seasons) with ectosymbiosis seemed more abundant during summer. Microscopic observations distinguished two main morphotypes of bacteria (rod-shaped and filamentous) on the cuticle of these nematodes, which seemed to be affiliated to Campylobacterota and Gammaproteobacteria, respectively. Both ectosymbionts belonged to clades of bacteria usually associated with invertebrates from deep-sea hydrothermal vents. The presence of the AprA gene involved in sulfur metabolism suggested a potential for chemosynthesis in the nematode microbial community. The discovery of potential symbiotic associations of a shallow-water organism with taxa usually associated with deep-sea hydrothermal vents, is new for Nematoda, opening new avenues for the study of ecology and bacterial relationships with meiofauna.

SUBMITTER: Bellec L

PROVIDER: S-EPMC6505526 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Chemosynthetic ectosymbionts associated with a shallow-water marine nematode.

Bellec Laure L Bonavita Marie-Anne Cambon MC Hourdez Stéphane S Jebbar Mohamed M Tasiemski Aurélie A Durand Lucile L Gayet Nicolas N Zeppilli Daniela D

Scientific reports 20190507 1

Prokaryotes and free-living nematodes are both very abundant and co-occur in marine environments, but little is known about their possible association. Our objective was to characterize the microbiome of a neglected but ecologically important group of free-living benthic nematodes of the Oncholaimidae family. We used a multi-approach study based on microscopic observations (Scanning Electron Microscopy and Fluorescence In Situ Hybridization) coupled with an assessment of molecular diversity usin ...[more]

PMID: 31065037

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Project description:Shallow-water hydrothermal systems represent extreme environments with unique biogeochemistry and high biological productivity, at which autotrophic microorganisms use both light and chemical energy for the production of biomass. Microbial communities of these ecosystems are metabolically diverse and possess the capacity to transform a large range of chemical compounds. Yet, little is known about their diversity or factors shaping their structure or how they compare to coastal sediments not impacted by hydrothermalism. To this end, we have used automated ribosomal intergenic spacer analysis (ARISA) and high-throughput Illumina sequencing combined with porewater geochemical analysis to investigate microbial communities along geochemical gradients in two shallow-water hydrothermal systems off the island of Dominica (Lesser Antilles). At both sites, venting of hydrothermal fluids substantially altered the porewater geochemistry by enriching it with silica, iron and dissolved inorganic carbon, resulting in island-like habitats with distinct biogeochemistry. The magnitude of fluid flow and difference in sediment grain size, which impedes mixing of the fluids with seawater, were correlated with the observed differences in the porewater geochemistry between the two sites. Concomitantly, individual sites harbored microbial communities with a significantly different community structure. These differences could be statistically linked to variations in the porewater geochemistry and the hydrothermal fluids. The two shallow-water hydrothermal systems of Dominica harbored bacterial communities with high taxonomical and metabolic diversity, predominated by heterotrophic microorganisms associated with the Gammaproteobacterial genera Pseudomonas and Pseudoalteromonas, indicating the importance of heterotrophic processes. Overall, this study shows that shallow-water hydrothermal systems contribute substantially to the biogeochemical heterogeneity and bacterial diversity of coastal sediments.

Project description:Eukaryotes may experience oxygen deprivation under several physiological and pathological conditions. Because oxygen shortage leads to a reduction in cellular energy production, all the eukaryotes studied so far evolved ways to conserve energy via suppression of metabolism. However, the molecular physiology of animals that naturally and repeatedly experience anoxia is poorly studied. One such animal is the symbiotic marine nematode Laxus oneistus. This thrives, invariably coated by its sulfur-oxidizing bacterium Candidatus Thiosymbion oneisti, in anoxic sulfidic or hypoxic sand. Here, by applying transcriptomics and proteomics, we discovered that, irrespective of the oxygen concentration it is subjected to, this nematode is mostly and constitutively engaging in ubiquitination-mediated proteolysis, energy generation, oxidative stress response and immune response. Furthermore, by incubating L. oneistus under sulfidic anoxic or hypoxic conditions, we found that, under the first condition, the worm upregulated genes involved in ribosome biogenesis, proteolytic systems (autophagy and the ubiquitin-proteasome system), chaperones, detoxification and lectins. Degradation pathways were likely induced to recycle damaged cellular components (mitochondria) and misfolded proteins into nutrients, whereas lectins were likely expressed to promote the attachment of its anaerobic, thiotrophic symbiont. Besides, L. oneistus appeared to survive oxygen deprivation by using alternative electron carriers (rhodoquinone) and acceptors (fumarate) to rewire the electron transfer chain. On the other hand, under hypoxia, genes involved in costly processes (e.g., development, amino acid biosynthesis, feeding behaviour, mating) were upregulated. Intriguingly, the worm’s Toll-like innate immunity pathway and a number of immune effectors (e.g., Bacterial Permeability Increasing proteins, fungicides) were upregulated in the presence of oxygen. In conclusion, we hypothesize that L. oneistus survives in anoxic sulfidic sand by overexpressing degradation processes, rewiring oxidative phosphorylation and by reinforcing its coat of bacterial sulfur-oxidizers. In the presence of oxygen, instead, it appears to exploit glycolysis to eat, mate and grow. Moreover, oxygen appears to affect L. oneistus immune system in such way, as to favor specific attachment of its anaerobic partner in anoxia and to produce broad-range antimicrobials when oxygen is present.

Dataset Information

Chemosynthetic ectosymbionts associated with a shallow-water marine nematode.

Publications

Chemosynthetic ectosymbionts associated with a shallow-water marine nematode.

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