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Genetic adaptations of sea anemone to hydrothermal environment.

ABSTRACT: Hydrothermal vent habitats are characterized by high hydrostatic pressure, darkness, and the continuous release of toxic metal ions into the surrounding environment where sea anemones and other invertebrates thrive. Nevertheless, the understanding of metazoan metal ion tolerances and environmental adaptations remains limited. We assembled a chromosome-level genome for the vent sea anemone, Alvinactis idsseensis sp. nov. Comparative genomic analyses revealed gene family expansions and gene innovations in A. idsseensis sp. nov. as a response to high concentrations of metal ions. Impressively, the metal tolerance proteins MTPs is a unique evolutionary response to the high concentrations of Fe²⁺ and Mn²⁺ present in the environments of these anemones. We also found genes associated with high concentrations of polyunsaturated fatty acids that may respond to high hydrostatic pressure and found sensory and circadian rhythm-regulated genes that were essential for adaptations to darkness. Overall, our results provide insights into metazoan adaptation to metal ions, high pressure, and darkness in hydrothermal vents.

SUBMITTER: Zhou Y

PROVIDER: S-EPMC10588955 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Genetic adaptations of sea anemone to hydrothermal environment.

Zhou Yang Y Liu Helu H Feng Chenguang C Lu Zaiqing Z Liu Jun J Huang Yanan Y Tang Huanhuan H Xu Zehui Z Pu Yujin Y Zhang Haibin H

Science advances 20231020 42

Hydrothermal vent habitats are characterized by high hydrostatic pressure, darkness, and the continuous release of toxic metal ions into the surrounding environment where sea anemones and other invertebrates thrive. Nevertheless, the understanding of metazoan metal ion tolerances and environmental adaptations remains limited. We assembled a chromosome-level genome for the vent sea anemone, <i>Alvinactis idsseensis</i> sp. nov. Comparative genomic analyses revealed gene family expansions and gene ...[more]

PMID: 37862424

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Project description:Hydrogenovibrio bacteria are ubiquitous in global deep-sea hydrothermal vents. However, their adaptations enabling survival in these harsh environments are not well understood. In this study, we characterized the physiology and metabolic mechanisms of Hydrogenovibrio thermophilus strain S5, which was first isolated from an active hydrothermal vent chimney on the Southwest Indian Ridge. Physiological characterizations showed that it is a microaerobic chemolithomixotroph that can utilize sulfide, thiosulfate, elemental sulfur, tetrathionate, thiocyanate or hydrogen as energy sources and molecular oxygen as the sole electron acceptor. During thiosulfate oxidation, the strain produced extracellular sulfur globules 0.7-6.0 μm in diameter that were mainly composed of elemental sulfur and carbon. Some organic substrates including amino acids, tryptone, yeast extract, casamino acids, casein, acetate, formate, citrate, propionate, tartrate, succinate, glucose and fructose can also serve as carbon sources, but growth is weaker than under CO2 conditions, indicating that strain S5 prefers to be chemolithoautotrophic. None of the tested organic carbons could function as energy sources. Growth tests under various conditions confirmed its adaption to a mesophilic mixing zone of hydrothermal vents in which vent fluid was mixed with cold seawater, preferring moderate temperatures (optimal 37°C), alkaline pH (optimal pH 8.0), microaerobic conditions (optimal 4% O2), and reduced sulfur compounds (e.g., sulfide, optimal 100 μM). Comparative genomics showed that strain S5 possesses more complex sulfur metabolism systems than other members of genus Hydrogenovibrio. The genes encoding the intracellular sulfur oxidation protein (DsrEF) and assimilatory sulfate reduction were first reported in the genus Hydrogenovibrio. In summary, the versatility in energy and carbon sources, and unique physiological properties of this bacterium have facilitated its adaptation to deep-sea hydrothermal vent environments.

Project description:Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis, an estuarine cnidarian. We sampled N. vectensis polyps from 5 different populations along a north-south gradient on the Atlantic coast of the United States and Canada. In addition, we sampled 3 populations at 3 different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for 1 month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by 4-fold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from 6 different populations in order to maintain each genotype at 3 different temperatures for 3 months. The bacterial community composition of the same N. vectensis clone differed greatly between the 3 different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N. vectensis. From our results we can conclude that N. vectensis-associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions.

Project description:BackgroundNumerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals. Despite success in nearly all marine habitats and their well-known associations with photosynthetic symbionts, Cnidaria remain one of the only phyla present in the deep-sea without a clearly documented example of dependence on chemosynthetic symbionts.ResultsA new chemosynthetic symbiosis between the sea anemone Ostiactis pearseae and intracellular bacteria was discovered at ~ 3700 m deep hydrothermal vents in the southern Pescadero Basin, Gulf of California. Unlike most sea anemones observed from chemically reduced habitats, this species was observed in and amongst vigorously venting fluids, side-by-side with the chemosynthetic tubeworm Oasisia aff. alvinae. Individuals of O. pearseae displayed carbon, nitrogen, and sulfur tissue isotope values suggestive of a nutritional strategy distinct from the suspension feeding or prey capture conventionally employed by sea anemones. Molecular and microscopic evidence confirmed the presence of intracellular SUP05-related bacteria housed in the tentacle epidermis of O. pearseae specimens collected from 5 hydrothermally active structures within two vent fields ~ 2 km apart. SUP05 bacteria (Thioglobaceae) dominated the O. pearseae bacterial community, but were not recovered from other nearby anemones, and were generally rare in the surrounding water. Further, the specific Ostiactis-associated SUP05 phylotypes were not detected in the environment, indicating a specific association. Two unusual candidate bacterial phyla (the OD1 and BD1-5 groups) appear to associate exclusively with O. pearseae and may play a role in symbiont sulfur cycling.ConclusionThe Cnidarian Ostiactis pearseae maintains a physical and nutritional alliance with chemosynthetic bacteria. The mixotrophic nature of this symbiosis is consistent with what is known about other cnidarians and the SUP05 bacterial group, in that they both form dynamic relationships to succeed in nature. The advantages gained by appropriating metabolic and structural resources from each other presumably contribute to their striking abundance in the Pescadero Basin, at the deepest known hydrothermal vents in the Pacific Ocean.

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Genetic adaptations of sea anemone to hydrothermal environment.

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Genetic adaptations of sea anemone to hydrothermal environment.

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