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Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs.

ABSTRACT: Hydrogen sulfide-rich groundwater discharges from springs into Lower Kane Cave, Wyoming, where microbial mats dominated by filamentous morphotypes are found. The full-cycle rRNA approach, including 16S rRNA gene retrieval and fluorescence in situ hybridization (FISH), was used to identify these filaments. The majority of the obtained 16S rRNA gene clones from the mats were affiliated with the "Epsilonproteobacteria" and formed two distinct clusters, designated LKC group I and LKC group II, within this class. Group I was closely related to uncultured environmental clones from petroleum-contaminated groundwater, sulfidic springs, and sulfidic caves (97 to 99% sequence similarity), while group II formed a novel clade moderately related to deep-sea hydrothermal vent symbionts (90 to 94% sequence similarity). FISH with newly designed probes for both groups specifically stained filamentous bacteria within the mats. FISH-based quantification of the two filament groups in six different microbial mat samples from Lower Kane Cave showed that LKC group II dominated five of the six mat communities. This study further expands our perceptions of the diversity and geographic distribution of "Epsilonproteobacteria" in extreme environments and demonstrates their biogeochemical importance in subterranean ecosystems.

SUBMITTER: Engel AS

PROVIDER: S-EPMC194925 | biostudies-literature | 2003 Sep

REPOSITORIES: biostudies-literature

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Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs.

Engel Annette Summers AS Lee Natuschka N Porter Megan L ML Stern Libby A LA Bennett Philip C PC Wagner Michael M

Applied and environmental microbiology 20030901 9

Hydrogen sulfide-rich groundwater discharges from springs into Lower Kane Cave, Wyoming, where microbial mats dominated by filamentous morphotypes are found. The full-cycle rRNA approach, including 16S rRNA gene retrieval and fluorescence in situ hybridization (FISH), was used to identify these filaments. The majority of the obtained 16S rRNA gene clones from the mats were affiliated with the "Epsilonproteobacteria" and formed two distinct clusters, designated LKC group I and LKC group II, withi ...[more]

PMID: 12957939

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Project description:Terrestrial sulfidic springs support diverse microbial communities by serving as stable conduits for geochemically diverse and nutrient-rich subsurface waters. Microorganisms that colonize terrestrial springs likely originate from groundwater, but may also be sourced from the surface. As such, the biogeographic distribution of microbial communities inhabiting sulfidic springs should be controlled by a combination of spring geochemistry and surface and subsurface transport mechanisms, and not necessarily geographic proximity to other springs. We examined the bacterial diversity of seven springs to test the hypothesis that occurrence of taxonomically similar microbes, important to the sulfur cycle, at each spring is controlled by geochemistry. Complementary Sanger sequencing and 454 pyrosequencing of 16S rRNA genes retrieved five proteobacterial classes, and Bacteroidetes, Chlorobi, Chloroflexi, and Firmicutes phyla from all springs, which suggested the potential for a core sulfidic spring microbiome. Among the putative sulfide-oxidizing groups (Epsilonproteobacteria and Gammaproteobacteria), up to 83% of the sequences from geochemically similar springs clustered together. Abundant populations of Hydrogenimonas-like or Sulfurovum-like spp. (Epsilonproteobacteria) occurred with abundant Thiothrix and Thiofaba spp. (Gammaproteobacteria), but Arcobacter-like and Sulfurimonas spp. (Epsilonproteobacteria) occurred with less abundant gammaproteobacterial populations. These distribution patterns confirmed that geochemistry rather than biogeography regulates bacterial dominance at each spring. Potential biogeographic controls were related to paleogeologic sedimentation patterns that could control long-term microbial transport mechanisms that link surface and subsurface environments. Knowing the composition of a core sulfidic spring microbial community could provide a way to monitor diversity changes if a system is threatened by anthropogenic processes or climate change.

Project description:The population genome of an uncultured bacterium assigned to the Campylobacterales (Epsilonproteobacteria) was reconstructed from a metagenome dataset obtained by whole-genome shotgun pyrosequencing. Genomic DNA was extracted from a sulfate-reducing, m-xylene-mineralizing enrichment culture isolated from groundwater of a benzene-contaminated sulfidic aquifer. The identical epsilonproteobacterial phylotype has previously been detected in toluene- or benzene-mineralizing, sulfate-reducing consortia enriched from the same site. Previous stable isotope probing (SIP) experiments with (13)C6-labeled benzene suggested that this phylotype assimilates benzene-derived carbon in a syntrophic benzene-mineralizing consortium that uses sulfate as terminal electron acceptor. However, the type of energy metabolism and the ecophysiological function of this epsilonproteobacterium within aromatic hydrocarbon-degrading consortia and in the sulfidic aquifer are poorly understood. Annotation of the epsilonproteobacterial population genome suggests that the bacterium plays a key role in sulfur cycling as indicated by the presence of an sqr gene encoding a sulfide quinone oxidoreductase and psr genes encoding a polysulfide reductase. It may gain energy by using sulfide or hydrogen/formate as electron donors. Polysulfide, fumarate, as well as oxygen are potential electron acceptors. Auto- or mixotrophic carbon metabolism seems plausible since a complete reductive citric acid cycle was detected. Thus the bacterium can thrive in pristine groundwater as well as in hydrocarbon-contaminated aquifers. In hydrocarbon-contaminated sulfidic habitats, the epsilonproteobacterium may generate energy by coupling the oxidation of hydrogen or formate and highly abundant sulfide with the reduction of fumarate and/or polysulfide, accompanied by efficient assimilation of acetate produced during fermentation or incomplete oxidation of hydrocarbons. The highly efficient assimilation of acetate was recently demonstrated by a pulsed (13)C2-acetate protein SIP experiment. The capability of nitrogen fixation as indicated by the presence of nif genes may provide a selective advantage in nitrogen-depleted habitats. Based on this metabolic reconstruction, we propose acetate capture and sulfur cycling as key functions of Epsilonproteobacteria within the intermediary ecosystem metabolism of hydrocarbon-rich sulfidic sediments.

Dataset Information

Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs.

Publications

Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs.

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