Metagenome Sequence Analysis of Filamentous Microbial Communities Obtained from Geochemically Distinct Geothermal Channels Reveals Specialization of Three Aquificales Lineages

Abstract

The Aquificales are thermophilic microorganisms that inhabit hydrothermal systems worldwide and are considered one of the earliest lineages of the domain Bacteria. We analyzed metagenome sequence obtained from six thermal “filamentous streamer” communities (∼40 Mbp per site), which targeted three different groups of Aquificales found in Yellowstone National Park (YNP). Unassembled metagenome sequence and PCR-amplified 16S rRNA gene libraries revealed that acidic, sulfidic sites were dominated by Hydrogenobaculum (Aquificaceae) populations, whereas the circum-neutral pH (6.5–7.8) sites containing dissolved sulfide were dominated by Sulfurihydrogenibium spp. (Hydrogenothermaceae). Thermocrinis (Aquificaceae) populations were found primarily in the circum-neutral sites with undetectable sulfide, and to a lesser extent in one sulfidic system at pH 8. Phylogenetic analysis of assembled sequence containing 16S rRNA genes as well as conserved protein-encoding genes revealed that the composition and function of these communities varied across geochemical conditions. Each Aquificales lineage contained genes for CO2 fixation by the reverse-TCA cycle, but only the Sulfurihydrogenibium populations perform citrate cleavage using ATP citrate lyase (Acl). The Aquificaceae populations use an alternative pathway catalyzed by two separate enzymes, citryl-CoA synthetase (Ccs), and citryl-CoA lyase (Ccl). All three Aquificales lineages contained evidence of aerobic respiration, albeit due to completely different types of heme Cu oxidases (subunit I) involved in oxygen reduction. The distribution of Aquificales populations and differences among functional genes involved in energy generation and electron transport is consistent with the hypothesis that geochemical parameters (e.g., pH, sulfide, H2, O2) have resulted in niche specialization among members of the Aquificales.

Hydrogen Peroxide Cycling in High-Temperature Acidic Geothermal Springs and Potential Implications for Oxidative Stress Response

“…Increases in O 2 during the day may in part be responsible for increases in microbial growth of M. yellowstonensis and Hydrogenobaculum, which are both aerobic (Kozubal et al, 2008;Takacs-Vesbach et al, 2013;Jennings et al, 2014). Higher 16S rRNA gene expression levels of Metallosphaera compared to Hydrogenobaculum in both environments ( Figure 5) were consistent with higher relative abundances of Metallosphaera observed previously in the upper ∼1 mm of mature Fe(III)-oxide mats, which also corresponds to the active O 2 -consuming layer (Beam et al, 2016).…”

“…The rod-shaped bacteria Hydrogenobaculum spp. initiate biofilm attachment, and the iron-oxidizing archaea Metallosphaera yellowstonensis (strain MK1) are responsible for the oxidation of Fe(II) and subsequent accretion of Fe(III)-oxides (Macur et al, 2004;Kozubal et al, 2008;Takacs-Vesbach et al, 2013;Jennings et al, 2014;Beam et al, 2016). Oxygen is a key driver of microbial growth and subsequent mat morphology (Kempes et al, 2014), and its diffusion into the mat is the rate-limiting factor for Fe(III)-oxide mat formation (Beam et al, 2016).…”

Metagenomics of microbial and viral life in terrestrial geothermal environments

“…Whereas the second one is represented in seven archaeal-dominated sediments: Nymph Lake (NL; 88°C, pH 4), Monarch Geyser (MG; 78-80°C, pH 4.0), Cistern Spring (CIS; 78-80°C, pH 4.4), Washburn Spring (WS; 76°C, pH 6.4), 100 Spring Plan (OSP_8; 72°C, pH 3.4), and including CH and JCHS described above (Inskeep et al 2013a, b). The diversity detected among sites with similar characteristics suggested that additional geochemical and geophysical factors, such as the total dissolved organic carbon (DOC) and the amount of solid-phases of carbon, could play a role in the consortia composition (Inskeep et al 2013a, b;Takacs-Vesbach et al 2013). A similar observation but mainly related to the different SO 4 2-/Cl -ratio was recently reported in the analysis of three thermal springs sharing pH * 4.0 of the YNP: Norris (NOR; 84°C, pH 4.34), Mary Bay Area (MRY; 80°C, pH 4.32) and Mud Kettles (MKL, 72°C pH 4.35), which resulted exclusively populated by bacteria and dominated by microorganisms belonging to the phylum of Cyanobacteria (NOR and MRY) and Aquificales (MKL) (Jiang and Takacs-Vesbach 2017).…”

Soil Microbial Responses to Increased Moisture and Organic Resources along a Salinity Gradient in a Polar Desert

“…Microbial communities in these habitats tend to have low diversity (2,4,5) and specialized physiologies (6), suggesting a potentially limited resistance and resilience to change (7). However, few experiments have been conducted in extreme environments to assess the susceptibility of these communities to disturbance.…”