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Metaproteogenomic Profiling of Chemosynthetic Microbial Biofilms Reveals Metabolic Flexibility During Colonization of a Shallow-Water Gas Vent.

ABSTRACT: Tor Caldara is a shallow-water gas vent located in the Mediterranean Sea, with active venting of CO₂ and H₂S. At Tor Caldara, filamentous microbial biofilms, mainly composed of Epsilon- and Gammaproteobacteria, grow on substrates exposed to the gas venting. In this study, we took a metaproteogenomic approach to identify the metabolic potential and in situ expression of central metabolic pathways at two stages of biofilm maturation. Our findings indicate that inorganic reduced sulfur species are the main electron donors and CO₂ the main carbon source for the filamentous biofilms, which conserve energy by oxygen and nitrate respiration, fix dinitrogen gas and detoxify heavy metals. Three metagenome-assembled genomes (MAGs), representative of key members in the biofilm community, were also recovered. Metaproteomic data show that metabolically active chemoautotrophic sulfide-oxidizing members of the Epsilonproteobacteria dominated the young microbial biofilms, while Gammaproteobacteria become prevalent in the established community. The co-expression of different pathways for sulfide oxidation by these two classes of bacteria suggests exposure to different sulfide concentrations within the biofilms, as well as fine-tuned adaptations of the enzymatic complexes. Taken together, our findings demonstrate a shift in the taxonomic composition and associated metabolic activity of these biofilms in the course of the colonization process.

SUBMITTER: Patwardhan S

PROVIDER: S-EPMC8056087 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Metaproteogenomic profiling of chemosynthetic microbial biofilms reveals metabolic flexibility during colonization of a shallow-water gas vent

Project description:Tor Caldara is a shallow-water gas vent located in the Mediterranean Sea, with active venting of CO 2 , H 2 S. At Tor Caldara, filamentous microbial biofilms, mainly composed of Epsilon- and Gammaproteobacteria, grow on substrates exposed to the gas venting. In this study, we took a metaproteogenomic approach to identify the metabolic potential and in situ expression of central metabolic pathways at two stages of biofilm maturation. Our findings indicate that inorganic reduced sulfur species are the main electron donors and CO 2 the main carbon source for the filamentous biofilms, which conserve energy by oxygen and nitrate respiration, fix dinitrogen gas and detoxify heavy metals. Three metagenome-assembled genomes (MAGs), representative of key members in the biofilm community, were also recovered. Metaproteomic data show that metabolically active chemoautotrophic sulfide-oxidizing members of the Epsilonproteobacteria dominated the young microbial biofilms, while Gammaproteobacteria become prevalent in the established community. The co-expression of different pathways for sulfide oxidation by these two classes of bacteria suggests exposure to different sulfide concentrations within the biofilms, as well as fine-tuned adaptations of the enzymatic complexes. Taken together, our findings demonstrate a shift in the taxonomic composition and associated metabolic activity of these biofilms in the course of the colonization process.

2021-01-25 | PXD023357 | Pride

Ecological Succession of Sulfur-Oxidizing Epsilon- and Gammaproteobacteria During Colonization of a Shallow-Water Gas Vent.

Project description:In this study, we integrated geochemical measurements, microbial diversity surveys and physiological characterization of laboratory strains to investigate substrate-attached filamentous microbial biofilms at Tor Caldara, a shallow-water gas vent in the Tyrrhenian Sea. At this site, the venting gases are mainly composed of CO2 and H2S and the temperature at the emissions is the same as that of the surrounding water. To investigate the composition of the total and active fraction of the Tor Caldara biofilm communities, we collected established and newly formed filaments and we sequenced the 16S rRNA genes (DNA) and the 16S rRNA transcripts (cDNA). Chemoautotrophic sulfur-oxidizing members of the Gammaproteobacteria (predominantly Thiotrichales) dominate the active fraction of the established microbial filaments, while Epsilonproteobacteria (predominantly Sulfurovum spp.) are more prevalent in the young filaments. This indicates a succession of the two communities, possibly in response to age, sulfide and oxygen concentrations. Growth experiments with representative laboratory strains in sulfide gradient medium revealed that Sulfurovum riftiae (Epsilonproteobacteria) grew closer to the sulfide source than Thiomicrospira sp. (Gammaproteobacteria, Thiotrichales). Overall, our findings show that sulfur-oxidizing Epsilonproteobacteria are the dominant pioneer colonizers of the Tor Caldara biofilm communities and that Gammaproteobacteria become prevalent once the community is established. This succession pattern appears to be driven - among other factors - by the adaptation of Epsilon- and Gammaproteobacteria to different sulfide concentrations.

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Microbial Communities of the Shallow-Water Hydrothermal Vent Near Naples, Italy, and Chemosynthetic Symbionts Associated With a Free-Living Marine Nematode.

Project description:Shallow-water hydrothermal vents are widespread, especially in the Mediterranean Sea, owing to the active volcanism of the area. Apart free microbial communities' investigations, few biological studies have been leaded yet. Investigations of microbial communities associated with Nematoda, an ecologically important group in sediments, can help to improve our overall understanding of these ecosystems. We used a multidisciplinary-approach, based on microscopic observations (scanning electron microscopy: SEM and Fluorescence In Situ Hybridization: FISH) coupled with a molecular diversity analysis using metabarcoding, based on the 16S rRNA gene (V3-V4 region), to characterize the bacterial community of a free-living marine nematode and its environment, the shallow hydrothermal vent near Naples (Italy). Observations of living bacteria in the intestine (FISH), molecular and phylogenetic analyses showed that this species of nematode harbors its own bacterial community, distinct from the surrounding sediment and water. Metabarcoding results revealed the specific microbiomes of the sediment from three sites of this hydrothermal area to be composed mainly of sulfur oxidizing and reducing related bacteria.

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Chemosynthetic ectosymbionts associated with a shallow-water marine nematode.

Project description: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.

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Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails.

Project description:Symbioses between invertebrate animals and chemosynthetic bacteria form the basis of hydrothermal vent ecosystems worldwide. In the Lau Basin, deep-sea vent snails of the genus Alviniconcha associate with either Gammaproteobacteria (A. kojimai, A. strummeri) or Campylobacteria (A. boucheti) that use sulfide and/or hydrogen as energy sources. While the A. boucheti host-symbiont combination (holobiont) dominates at vents with higher concentrations of sulfide and hydrogen, the A. kojimai and A. strummeri holobionts are more abundant at sites with lower concentrations of these reductants. We posit that adaptive differences in symbiont physiology and gene regulation might influence the observed niche partitioning between host taxa. To test this hypothesis, we used high-pressure respirometers to measure symbiont metabolic rates and examine changes in gene expression among holobionts exposed to in situ concentrations of hydrogen (H2: ~25?µM) or hydrogen sulfide (H2S: ~120?µM). The campylobacterial symbiont exhibited the lowest rate of H2S oxidation but the highest rate of H2 oxidation, with fewer transcriptional changes and less carbon fixation relative to the gammaproteobacterial symbionts under each experimental condition. These data reveal potential physiological adaptations among symbiont types, which may account for the observed net differences in metabolic activity and contribute to the observed niche segregation among holobionts.

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Mapping the resilience of chemosynthetic communities in hydrothermal vent fields.

Project description:Hydrothermal vent fields are vulnerable to natural disturbances, such as volcanic activity, and are currently being considered as targets for mineral mining. Local vent communities are linked by pelagic larval dispersal and form regional metacommunities, nested within a number of biogeographic provinces. Larval supply depends on the connectivity of the dispersal networks, and affects recoverability of communities from disturbances. However, it is unclear how the dispersal networks contribute to recoverability of local communities. Here, we integrated a population dynamics model and estimation of large scale dispersal networks. By simulating disturbances to vent fields, we mapped recoverability of communities in 131 hydrothermal vent fields in the western Pacific Ocean. Our analysis showed substantial variation in recovery time due to variation in regional connectivity between known vent fields, and was not qualitatively affected by potential larval recruitment from unknown vent fields. In certain cases, simultaneous disturbance of a series of vent fields either delayed or wholly prevented recovery. Our approach is applicable to a dispersal network estimated from genetic diversity. Our method not only reveals distribution of recoverability of chemosynthetic communities in hydrothermal vent fields, but is also a practical tool for planning conservation strategies.

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Diversity and phylogenetic analyses of bacteria from a shallow-water hydrothermal vent in Milos island (Greece).

Project description:Studies of shallow-water hydrothermal vents have been lagging behind their deep-sea counterparts. Hence, the importance of these systems and their contribution to the local and regional diversity and biogeochemistry is unclear. This study analyzes the bacterial community along a transect at the shallow-water hydrothermal vent system of Milos island, Greece. The abundance and biomass of the prokaryotic community is comparable to areas not affected by hydrothermal activity and was, on average, 1.34 × 10(8) cells g(-1). The abundance, biomass and diversity of the prokaryotic community increased with the distance from the center of the vent and appeared to be controlled by the temperature gradient rather than the trophic conditions. The retrieved 16S rRNA gene fragments matched sequences from a variety of geothermal environments, although the average similarity was low (94%), revealing previously undiscovered taxa. Epsilonproteobacteria constituted the majority of the population along the transect, with an average contribution to the total diversity of 60%. The larger cluster of 16S rRNA gene sequences was related to chemolithoautotrophic Sulfurovum spp., an Epsilonproteobacterium so far detected only at deep-sea hydrothermal vents. The presence of previously unknown lineages of Epsilonproteobacteria could be related to the abundance of organic matter in these systems, which may support alternative metabolic strategies to chemolithoautotrophy. The relative contribution of Gammaproteobacteria to the Milos microbial community increased along the transect as the distance from the center of the vent increased. Further attempts to isolate key species from these ecosystems will be critical to shed light on their evolution and ecology.

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Trophic structure and energy flow in a shallow-water hydrothermal vent: Insights from a stable isotope approach.

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