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Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean.

ABSTRACT: Here we describe novel forms of structural integration between endo- and episymbiotic microbes and an unusual new species of snail from hydrothermal vents in the Indian Ocean. The snail houses a dense population of gamma-proteobacteria within the cells of its greatly enlarged esophageal gland. This tissue setting differs from that of all other vent mollusks, which harbor sulfur-oxidizing endosymbionts in their gills. The significantly reduced digestive tract, the isotopic signatures of the snail tissues, and the presence of internal bacteria suggest a dependence on chemoautotrophy for nutrition. Most notably, this snail is unique in having a dense coat of mineralized scales covering the sides of its foot, a feature seen in no other living metazoan. The scales are coated with iron sulfides (pyrite and greigite) and heavily colonized by epsilon- and delta-proteobacteria, likely participating in mineralization of the sclerites. This novel metazoan-microbial collaboration illustrates the great potential of organismal adaptation in chemically and physically challenging deep-sea environments.

SUBMITTER: Goffredi SK

PROVIDER: S-EPMC404406 | biostudies-literature | 2004 May

REPOSITORIES: biostudies-literature

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Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean.

Goffredi Shana K SK Warén Anders A Orphan Victoria J VJ Van Dover Cindy L CL Vrijenhoek Robert C RC

Applied and environmental microbiology 20040501 5

Here we describe novel forms of structural integration between endo- and episymbiotic microbes and an unusual new species of snail from hydrothermal vents in the Indian Ocean. The snail houses a dense population of gamma-proteobacteria within the cells of its greatly enlarged esophageal gland. This tissue setting differs from that of all other vent mollusks, which harbor sulfur-oxidizing endosymbionts in their gills. The significantly reduced digestive tract, the isotopic signatures of the snail ...[more]

PMID: 15128570

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Project description:The hydrothermal-vent gastropod Alviniconcha aff. hessleri from the Kairei hydrothermal field on the Central Indian Ridge houses bacterium-like cells internally in its greatly enlarged gill. A single 16S rRNA gene sequence was obtained from the DNA extract of the gill, and phylogenetic analysis placed the source organism within a lineage of the epsilon subdivision of the Proteobacteria. Fluorescence in situ hybridization analysis with an oligonucleotide probe targeting the specific epsilonproteobacterial subgroup showed the bacterium densely colonizing the gill filaments. Carbon isotopic homogeneity among the gastropod tissue parts, regardless of the abundance of the endosymbiont cells, suggests that the carbon isotopic composition of the endosymbiont biomass is approximately the same as that of the gastropod. Compound-specific carbon isotopic analysis revealed that fatty acids from the gastropod tissues are all (13)C enriched relative to the gastropod biomass and that the monounsaturated C(16) fatty acid that originates from the endosymbiont is as (13)C enriched relative to the gastropod biomass as that of the epsilonproteobacterial cultures grown under chemoautotrophic conditions. This fractionation pattern is most likely due to chemoautotrophy based on the reductive tricarboxylic-acid (rTCA) cycle and subsequent fatty acid biosynthesis from (13)C-enriched acetyl coenzyme A. Enzymatic characterization revealed evident activity of several key enzymes of the rTCA cycle, as well as the absence of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in the gill tissue. The results from anatomic, molecular phylogenetic, bulk and compound-specific carbon isotopic, and enzymatic analyses all support the inference that a novel nutritional strategy relying on chemoautotrophy in the epsilonproteobacterial endosymbiont is utilized by the hydrothermal-vent gastropod from the Indian Ocean. The discrepancies between the data of the present study and those of previous ones for Alviniconcha gastropods from the Pacific Ocean imply that at least two lineages of chemoautotrophic bacteria, phylogenetically distinct at the subdivision level, occur as the primary endosymbiont in one host animal type.

Project description:In the ocean, viruses impact microbial mortality, regulate biogeochemical cycling, and alter the metabolic potential of microbial lineages. At deep-sea hydrothermal vents, abundant viruses infect a wide range of hosts among the archaea and bacteria that inhabit these dynamic habitats. However, little is known about viral diversity, host range, and biogeography across different vent ecosystems, which has important implications for how viruses manipulate microbial function and evolution. Here, we examined viral diversity, viral and host distribution, and virus-host interactions in microbial metagenomes generated from venting fluids from several vent sites within three different geochemically and geographically distinct hydrothermal systems: Piccard and Von Damm vent fields at the Mid-Cayman Rise in the Caribbean Sea, and at several vent sites within Axial Seamount in the Pacific Ocean. Analysis of viral sequences and clustered regularly interspaced short palindromic repeat (CRISPR) spacers revealed highly diverse viral assemblages and evidence of active infection. Network analysis revealed that viral host range was relatively narrow, with very few viruses infecting multiple microbial lineages. Viruses were largely endemic to individual vent sites, indicating restricted dispersal, and in some cases, viral assemblages persisted over time. Thus, we show that hydrothermal vent fluids are home to novel, diverse viral assemblages that are highly localized to specific regions and taxa. IMPORTANCE Viruses play important roles in manipulating microbial communities and their evolution in the ocean, yet not much is known about viruses in deep-sea hydrothermal vents. However, viral ecology and evolution are of particular interest in hydrothermal vent habitats because of their unique nature: previous studies have indicated that most viruses in hydrothermal vents are temperate rather than lytic, and it has been established that rates of horizontal gene transfer (HGT) are particularly high among thermophilic vent microbes, and viruses are common vectors for HGT. If viruses have broad host range or are widespread across vent sites, they have increased potential to act as gene-sharing "highways" between vent sites. By examining viral diversity, distribution, and infection networks across disparate vent sites, this study provides the opportunity to better characterize and constrain the viral impact on hydrothermal vent microbial communities. We show that viruses in hydrothermal vents are diverse and apparently active, but most have restricted host range and are not widely distributed among vent sites. Thus, the impacts of viral infection are likely to be highly localized and constrained to specific taxa in these habitats.

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Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean.

Publications

Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean.

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