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  • 1
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    PANGAEA
    In:  Supplement to: Rubin-Blum, Maxim; Antony, Chakkiath Paul; Sayavedra, Lizbeth; Martínez-Pérez, Clara; Birgel, Daniel; Peckmann, Jörn; Wu, Yu-Chen; Cárdenas, Paco; MacDonald, Ian R; Marcon, Yann; Sahling, Heiko; Hentschel, Ute; Dubilier, Nicole (2019): Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts. The ISME Journal, https://doi.org/10.1038/s41396-019-0346-7
    Publication Date: 2023-11-20
    Description: Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host–symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea.
    Keywords: asphalt; Center for Marine Environmental Sciences; Chapopote; Gulf of Mexico; LAPM; MARUM; Mosaic; Photomosaic; seep; TAR
    Type: Dataset
    Format: application/zip, 2 datasets
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  • 2
    Publication Date: 2023-11-20
    Keywords: asphalt; Center for Marine Environmental Sciences; Chapopote; File content; File format; File name; File size; Gulf of Mexico; LAPM; MARUM; Mosaic; Photomosaic; seep; TAR; Uniform resource locator/link to file
    Type: Dataset
    Format: text/tab-separated-values, 20 data points
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  • 3
    Publication Date: 2021-05-07
    Description: Highlights: • Mid-Atlantic vent mussel populations are contemporarily isolated • Population connectivity can only be maintained in a stepwise manner • Four mussel lineages exist on the Mid-Atlantic Ridge • Recolonization of perturbed vent localities is uncertain Summary: Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats (“phantom” stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas.
    Type: Article , PeerReviewed
    Format: text
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  • 4
    Publication Date: 2019-01-22
    Description: Bathymodiolus mussels live in symbiosis with intracellular sulfur-oxidizing (SOX) bacteria that provide them with nutrition. We sequenced the SOX symbiont genomes from two Bathymodiolus species. Comparison of these symbiont genomes with those of their closest relatives revealed that the symbionts have undergone genome rearrangements, and up to 35% of their genes may have been acquired by horizontal gene transfer. Many of the genes specific to the symbionts were homologs of virulence genes. We discovered an abundant and diverse array of genes similar to insecticidal toxins of nematode and aphid symbionts, and toxins of pathogens such as Yersinia and Vibrio. Transcriptomics and proteomics revealed that the SOX symbionts express the toxin-related genes (TRGs) in their hosts. We hypothesize that the symbionts use these TRGs in beneficial interactions with their host, including protection against parasites. This would explain why a mutualistic symbiont would contain such a remarkable 'arsenal' of TRGs
    Type: Article , PeerReviewed
    Format: text
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  • 5
    Publication Date: 2022-01-31
    Description: Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host–symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
    Format: text
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    Format: other
    Format: other
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  • 6
    Publication Date: 2020-02-14
    Description: Genetic diversity of closely related free-living microorganisms is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Accordingly, strain diversity is assumed to be highly restricted in intracellular bacteria associated with animals. Here, we sequenced metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key functions, such as the use of energy and nutrient sources, electron acceptors and viral defence mechanisms. Most strain-specific genes were expressed, highlighting their potential to affect fitness. We show that fine-scale diversity is pervasive in Bathymodiolus sulfur-oxidizing symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, rather than the host, feeds the symbionts.
    Repository Name: EPIC Alfred Wegener Institut
    Type: Article , isiRev , info:eu-repo/semantics/article
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  • 7
    Publication Date: 2021-09-25
    Description: Genetic diversity of closely related free-living microorganisms is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Accordingly, strain diversity is assumed to be highly restricted in intracellular bacteria associated with animals. Here, we sequenced metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key functions, such as the use of energy and nutrient sources, electron acceptors and viral defence mechanisms. Most strain-specific genes were expressed, highlighting their potential to affect fitness. We show that fine-scale diversity is pervasive in Bathymodiolus sulfur-oxidizing symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, rather than the host, feeds the symbionts.
    Repository Name: EPIC Alfred Wegener Institut
    Type: Article , peerRev , info:eu-repo/semantics/article
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  • 8
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Ponnudurai, R., Heiden, S. E., Sayavedra, L., Hinzke, T., Kleiner, M., Hentschker, C., Felbeck, H., Sievert, S. M., Schlüter, R., Becher, D., Schweder, T., & Markert, S. Comparative proteomics of related symbiotic mussel species reveals high variability of host-symbiont interactions. ISME Journal, 14, (2019): 649–656, doi: 10.1038/s41396-019-0517-6.
    Description: Deep-sea Bathymodiolus mussels and their chemoautotrophic symbionts are well-studied representatives of mutualistic host–microbe associations. However, how host–symbiont interactions vary on the molecular level between related host and symbiont species remains unclear. Therefore, we compared the host and symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic symbiont, and Atlantic B. azoricus, containing two symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic symbionts, and a cycling mechanism that could supply the host with symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus symbiont. These findings imply that host–microbe interactions can be quite variable, even between closely related systems.
    Description: Thanks to captain, crew, and pilots of the research vessels Atlantis (ROV Jason cruise AT26–10 in 2014) and Meteor (cruise M82–3 in 2010). We thank Jana Matulla, Sebastian Grund, and Annette Meuche for excellent technical assistance during sample preparation, MS measurements in the Orbitrap Classic, and TEM imaging preparation, respectively. We appreciate Nikolaus Leisch’s help with TEM image interpretation, Inna Sokolova’s advice on bivalve physiology, and Marie Zühlke’s support during manuscript revision. RP was supported by the EU-funded Marie Curie Initial Training Network ‘Symbiomics’ (project no. 264774) and by a fellowship of the Institute of Marine Biotechnology e.V. TH was supported by the German Research Foundation DFG (grant MA 6346/2–1 to SM). The Atlantis cruise was funded by a grant of the US National Science Foundation’s Dimensions of Biodiversity program to SMS (OCE-1136727).
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 9
    Publication Date: 2022-05-26
    Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Standards in Genomic Sciences 12 (2017): 50, doi:10.1186/s40793-017-0266-y.
    Description: Bathymodiolus thermophilus, a mytilid mussel inhabiting the deep-sea hydrothermal vents of the East Pacific Rise, lives in symbiosis with chemosynthetic Gammaproteobacteria within its gills. The intracellular symbiont population synthesizes nutrients for the bivalve host using the reduced sulfur compounds emanating from the vents as energy source. As the symbiont is uncultured, comprehensive and detailed insights into its metabolism and its interactions with the host can only be obtained from culture-independent approaches such as genomics and proteomics. In this study, we report the first draft genome sequence of the sulfur-oxidizing symbiont of B. thermophilus, here tentatively named Candidatus Thioglobus thermophilus. The draft genome (3.1 Mb) harbors 3045 protein-coding genes. It revealed pathways for the use of sulfide and thiosulfate as energy sources and encodes the Calvin-Benson-Bassham cycle for CO2 fixation. Enzymes required for the synthesis of the tricarboxylic acid cycle intermediates oxaloacetate and succinate were absent, suggesting that these intermediates may be substituted by metabolites from external sources. We also detected a repertoire of genes associated with cell surface adhesion, bacteriotoxicity and phage immunity, which may perform symbiosis-specific roles in the B. thermophilus symbiosis.
    Description: This study was supported by the EU-funded Marie Curie Initial Training Network “Symbiomics” (project no. 264774). RP was supported by a fellowship of the Institute of Marine Biotechnology, Greifswald. MK was supported by a NSERC Banting Postdoctoral Fellowship. LS was supported by a DAAD scholarship. SMS was supported by US National Science Foundation grant OCE-1136727.
    Keywords: Uncultured endosymbiont ; Hydrothermal vents ; Marine invertebrate symbiosis ; Thiotrophy ; Autotrophy ; Atlantis (Ship : 1996-) Cruise AT26-10
    Repository Name: Woods Hole Open Access Server
    Type: Article
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