Dataset Information

Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats.

ABSTRACT: The evolutionarily ancient Aquificales bacterium Sulfurihydrogenibium spp. dominates filamentous microbial mat communities in shallow, fast-flowing, and dysoxic hot-spring drainage systems around the world. In the present study, field observations of these fettuccini-like microbial mats at Mammoth Hot Springs in Yellowstone National Park are integrated with geology, geochemistry, hydrology, microscopy, and multi-omic molecular biology analyses. Strategic sampling of living filamentous mats along with the hot-spring CaCO3 (travertine) in which they are actively being entombed and fossilized has permitted the first direct linkage of Sulfurihydrogenibium spp. physiology and metabolism with the formation of distinct travertine streamer microbial biomarkers. Results indicate that, during chemoautotrophy and CO2 carbon fixation, the 87-98% Sulfurihydrogenibium-dominated mats utilize chaperons to facilitate enzyme stability and function. High-abundance transcripts and proteins for type IV pili and extracellular polymeric substances (EPSs) are consistent with their strong mucus-rich filaments tens of centimeters long that withstand hydrodynamic shear as they become encrusted by more than 5?mm of travertine per day. Their primary energy source is the oxidation of reduced sulfur (e.g., sulfide, sulfur, or thiosulfate) and the simultaneous uptake of extremely low concentrations of dissolved O2 facilitated by bd-type cytochromes. The formation of elevated travertine ridges permits the Sulfurihydrogenibium-dominated mats to create a shallow platform from which to access low levels of dissolved oxygen at the virtual exclusion of other microorganisms. These ridged travertine streamer microbial biomarkers are well preserved and create a robust fossil record of microbial physiological and metabolic activities in modern and ancient hot-spring ecosystems.

SUBMITTER: Dong Y

PROVIDER: S-EPMC6918859 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats.

Dong Yiran Y Sanford Robert A RA Inskeep William P WP Srivastava Vaibhav V Bulone Vincent V Fields Christopher J CJ Yau Peter M PM Sivaguru Mayandi M Ahrén Dag D Fouke Kyle W KW Weber Joseph J Werth Charles R CR Cann Isaac K IK Keating Kathleen M KM Khetani Radhika S RS Hernandez Alvaro G AG Wright Chris C Band Mark M Imai Brian S BS Fried Glenn A GA Fouke Bruce W BW

Astrobiology 20190430 12

The evolutionarily ancient Aquificales bacterium <i>Sulfurihydrogenibium</i> spp. dominates filamentous microbial mat communities in shallow, fast-flowing, and dysoxic hot-spring drainage systems around the world. In the present study, field observations of these fettuccini-like microbial mats at Mammoth Hot Springs in Yellowstone National Park are integrated with geology, geochemistry, hydrology, microscopy, and multi-omic molecular biology analyses. Strategic sampling of living filamentous mat ...[more]

PMID: 31038352

Similar Datasets

Project description:The Sembawang Hot Spring in Singapore lies at the foot of a major regional geological feature called the Bentong-Raub Suture Zone. Amid an extensively managed surface geothermal park, an undisturbed hot spring emerges with source water at 61°C, pH 6.8, and 1 mg/L dissolved sulfide. A small main pool at the source supported orange-green benthic flocs, whereas the outflow channel with gradually less extreme environmental stress supported extensive vivid green microbial mats. Microscopy revealed that cyanobacterial morphotypes were distinct in flocs and mats at several intervals along the environmental gradient, and we describe a spiraling pattern in the oscillatorian cyanobacteria that may reflect response to poly-extreme stress. Estimation of diversity using 16S rRNA gene sequencing revealed assemblages that were dominated by phototrophic bacteria. The most abundant taxa in flocs at 61°C/1 mg/L sulfide were Roseiflexus sp. and Thermosynechococcus elongatus, whilst the mats at 45.7-55.3°C/0-0.5 mg/L sulfide were dominated by Oscillatoriales cyanobacterium MTP1 and Chloroflexus sp. Occurrence of diverse chemoautotrophs and heterotrophs reflected known thermal ranges for taxa, and of note was the high abundance of thermophilic cellulolytic bacteria that likely reflected the large allochthonous leaf input. A clear shift in ASV-defined putative ecotypes occurred along the environmental stress gradient of the hot spring and overall diversity was inversely correlated to environmental stress. Significant correlations for abiotic variables with observed biotic diversity were identified for temperature, sulfide, and carbonate. A network analysis revealed three putative modules of biotic interactions that also reflected the taxonomic composition at intervals along the environmental gradient. Overall, the data indicated that three distinct microbial communities were supported within a small spatial scale along the poly-extreme environmental gradient. The findings add to the growing inventory of hot spring microbiomes and address an important biogeographic knowledge gap for the region.

Project description:Viruses exert diverse ecosystem impacts by controlling their host community through lytic predator-prey dynamics. However, the mechanisms by which lysogenic viruses influence their host-microbial community are less clear. In hot springs, lysogeny is considered an active lifestyle, yet it has not been systematically studied in all habitats, with phototrophic microbial mats (PMMs) being particularly not studied. We carried out viral metagenomics following in situ mitomycin C induction experiments in PMMs from Porcelana hot spring (Northern Patagonia, Chile). The compositional changes of viral communities at two different sites were analyzed at the genomic and gene levels. Furthermore, the presence of integrated prophage sequences in environmental metagenome-assembled genomes from published Porcelana PMM metagenomes was analyzed. Our results suggest that virus-specific replicative cycles (lytic and lysogenic) were associated with specific host taxa with different metabolic capacities. One of the most abundant lytic viral groups corresponded to cyanophages, which would infect the cyanobacteria Fischerella, the most active and dominant primary producer in thermophilic PMMs. Likewise, lysogenic viruses were related exclusively to chemoheterotrophic bacteria from the phyla Proteobacteria, Firmicutes, and Actinobacteria. These temperate viruses possess accessory genes to sense or control stress-related processes in their hosts, such as sporulation and biofilm formation. Taken together, these observations suggest a nexus between the ecological role of the host (metabolism) and the type of viral lifestyle in thermophilic PMMs. This has direct implications in viral ecology, where the lysogenic-lytic switch is determined by nutrient abundance and microbial density but also by the metabolism type that prevails in the host community. IMPORTANCE Hot springs harbor microbial communities dominated by a limited variety of microorganisms and, as such, have become a model for studying community ecology and understanding how biotic and abiotic interactions shape their structure. Viruses in hot springs are shown to be ubiquitous, numerous, and active components of these communities. However, lytic and lysogenic viral communities of thermophilic phototrophic microbial mats (PMMs) remain largely unexplored. In this work, we use the power of viral metagenomics to reveal changes in the viral community following a mitomycin C induction experiment in PMMs. The importance of our research is that it will improve our understanding of viral lifestyles in PMMs via exploring the differences in the composition of natural and induced viral communities at the genome and gene levels. This novel information will contribute to deciphering which biotic and abiotic factors may control the transitions between lytic and lysogenic cycles in these extreme environments.

Dataset Information

Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats.

Publications

Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets