Abstract
Thermal spring ecosystems are a valuable resource for the discovery of novel hyperthermophilic Bacteria and Archaea, and harbor deeply-branching lineages that provide insight regarding the nature of early microbial life. We characterized bacterial populations in two circumneutral (pH ~8) Yellowstone National Park thermal (T ~80°C) spring filamentous “streamer” communities using random metagenomic DNA sequence to investigate the metabolic potential of these novel populations. Four de novo assemblies representing three abundant, deeply-branching bacterial phylotypes were recovered. Analysis of conserved phylogenetic marker genes indicated that two of the phylotypes represent separate groups of an uncharacterized phylum (for which we propose the candidate phylum name “Pyropristinus”). The third new phylotype falls within the proposed Calescamantes phylum. Metabolic reconstructions of the “Pyropristinus” and Calescamantes populations showed that these organisms appear to be chemoorganoheterotrophs and have the genomic potential for aerobic respiration and oxidative phosphorylation via archaeal-like V-type, and bacterial F-type ATPases, respectively. A survey of similar phylotypes (>97% nt identity) within 16S rRNA gene datasets suggest that the newly described organisms are restricted to terrestrial thermal springs ranging from 70 to 90°C and pH values of ~7–9. The characterization of these lineages is important for understanding the diversity of deeply-branching bacterial phyla, and their functional role in high-temperature circumneutral “streamer” communities.
Highlights
The discovery and characterization of early-branching lineages of Bacteria and Archaea has been crucial for studying the origin and evolution of life on Earth
The average coverage, G+C content (%), and cumulative sequence plots of contigs corresponding to the three “Pyropristinus” (T1.1, Type 1 (T1).2, Type 2 (T2)), and the Calescamantes populations are provided in supplemental information (Supplemental Figure 1)
A G+C (%) frequency plot of random metagenome sequence reads that were phylogenetically assigned (>90% nucleotide identity) to the de novo assemblies compiled from these sites showed that “Pyropristinus” T1 and T2, as well as the Calescamantes-like phylotypes were significant members (∼7–8% of all reads) of the more even microbial community in Octopus Spring, and that the “Pyropristinus” T1 was abundant (∼12%) in Bechler spring (Figure 2, Table 1)
Summary
The discovery and characterization of early-branching lineages of Bacteria and Archaea has been crucial for studying the origin and evolution of life on Earth. Hyperthermophiles inhabit geothermal environments that are analogous to those of early Earth (Baross and Hoffman, 1985), and are generally the deepest branching representatives of the tree of Life (Di Giulio, 2003; Stetter, 2006). Novel Deep-Branching Thermophilic Bacteria and Thermotogae have been considered the most basal bacterial lineages on the basis of phylogenetic evidence (Barion et al, 2007; Zhaxybayeva et al, 2009). Discovery and characterization of new and uncultured lineages of thermophilic microorganisms are extremely useful toward the broader goal of understanding genomic and metabolic attributes of deep-branching phyla, which inhabit modern-day environments that may be analogs to those potentially important in the origin(s) of life
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