Predominant Acidilobus-Like Populations from Geothermal Environments in Yellowstone National Park Exhibit Similar Metabolic Potential in Different Hypoxic Microbial Communities
Abstract:c High-temperature (>70°C) ecosystems in Yellowstone National Park (YNP) provide an unparalleled opportunity to study chemotrophic archaea and their role in microbial community structure and function under highly constrained geochemical conditions. Acidilobus spp. (order Desulfurococcales) comprise one of the dominant phylotypes in hypoxic geothermal sulfur sediment and Fe(III)-oxide environments along with members of the Thermoproteales and Sulfolobales. Consequently, the primary goals of the current study we… Show more
“…Other archaea present in these communities include members of two novel archaeal groups, the Thaumarchaeota and the Euryarchaeota (Thermoplasmatales-like), as well as other crenarchaea within the orders Thermoproteales and Desulfurococcales (19,24,25). However, sequence assemblies corresponding to these populations do not contain evidence of marker genes for known CO 2 fixation pathways and appear to be primarily heterotrophic (18,19,24,25,37,41). Despite the diversity of archaea in these Fe(II)-oxidizing communities, the only known CO 2 fixation pathways found in metagenome sequence analyses included the 3-HP/4-HB pathway (contributed by M. yellowstonensis-like and other Sulfolobales populations) and the r-TCA cycle (contributed by Hydrogenobaculum-like populations).…”
The fixation of inorganic carbon has been documented in all three domains of life and results in the biosynthesis of diverse organic compounds that support heterotrophic organisms. The primary aim of this study was to assess carbon dioxide fixation in high-temperature Fe(III)-oxide mat communities and in pure cultures of a dominant Fe(II)-oxidizing organism (Metallosphaera yellowstonensis strain MK1) originally isolated from these environments. Protein-encoding genes of the complete 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB) carbon dioxide fixation pathway were identified in M. yellowstonensis strain MK1. Highly similar M. yellowstonensis genes for this pathway were identified in metagenomes of replicate Fe(III)-oxide mats, as were genes for the reductive tricarboxylic acid cycle from Hydrogenobaculum spp. (Aquificales). Stable-isotope ( 13 CO 2 ) labeling demonstrated CO 2 fixation by M. yellowstonensis strain MK1 and in ex situ assays containing live Fe(III)-oxide microbial mats. The results showed that strain MK1 fixes CO 2 with a fractionation factor of ϳ2.5‰. Analysis of the 13 C composition of dissolved inorganic C (DIC), dissolved organic C (DOC), landscape C, and microbial mat C showed that mat C is from both DIC and non-DIC sources. An isotopic mixing model showed that biomass C contains a minimum of 42% C of DIC origin, depending on the fraction of landscape C that is present. The significance of DIC as a major carbon source for Fe(III)-oxide mat communities provides a foundation for examining microbial interactions that are dependent on the activity of autotrophic organisms (i.e., Hydrogenobaculum and Metallosphaera spp.) in simplified natural communities.
“…Other archaea present in these communities include members of two novel archaeal groups, the Thaumarchaeota and the Euryarchaeota (Thermoplasmatales-like), as well as other crenarchaea within the orders Thermoproteales and Desulfurococcales (19,24,25). However, sequence assemblies corresponding to these populations do not contain evidence of marker genes for known CO 2 fixation pathways and appear to be primarily heterotrophic (18,19,24,25,37,41). Despite the diversity of archaea in these Fe(II)-oxidizing communities, the only known CO 2 fixation pathways found in metagenome sequence analyses included the 3-HP/4-HB pathway (contributed by M. yellowstonensis-like and other Sulfolobales populations) and the r-TCA cycle (contributed by Hydrogenobaculum-like populations).…”
The fixation of inorganic carbon has been documented in all three domains of life and results in the biosynthesis of diverse organic compounds that support heterotrophic organisms. The primary aim of this study was to assess carbon dioxide fixation in high-temperature Fe(III)-oxide mat communities and in pure cultures of a dominant Fe(II)-oxidizing organism (Metallosphaera yellowstonensis strain MK1) originally isolated from these environments. Protein-encoding genes of the complete 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB) carbon dioxide fixation pathway were identified in M. yellowstonensis strain MK1. Highly similar M. yellowstonensis genes for this pathway were identified in metagenomes of replicate Fe(III)-oxide mats, as were genes for the reductive tricarboxylic acid cycle from Hydrogenobaculum spp. (Aquificales). Stable-isotope ( 13 CO 2 ) labeling demonstrated CO 2 fixation by M. yellowstonensis strain MK1 and in ex situ assays containing live Fe(III)-oxide microbial mats. The results showed that strain MK1 fixes CO 2 with a fractionation factor of ϳ2.5‰. Analysis of the 13 C composition of dissolved inorganic C (DIC), dissolved organic C (DOC), landscape C, and microbial mat C showed that mat C is from both DIC and non-DIC sources. An isotopic mixing model showed that biomass C contains a minimum of 42% C of DIC origin, depending on the fraction of landscape C that is present. The significance of DIC as a major carbon source for Fe(III)-oxide mat communities provides a foundation for examining microbial interactions that are dependent on the activity of autotrophic organisms (i.e., Hydrogenobaculum and Metallosphaera spp.) in simplified natural communities.
“…Ferric iron concentrations were then calculated as the difference between total soluble iron and ferrous iron. Total dissolved sulfide (TS) was assessed using the amine sulfuric acid method (APHA, 1998;Macur et al, 2013;Jay et al, 2014) with 7.5 mL of unfiltered samples [to avoid rapid degassing of H 2 S(aq) upon filtration].…”
Section: Aqueous Geochemistry Of Geothermal Springsmentioning
Hydrogen peroxide (H 2 O 2 ), superoxide (O •−2 ), and hydroxyl radicals (OH • ) are produced in natural waters via ultraviolet (UV) light-induced reactions between dissolved oxygen (O 2 ) and organic carbon, and further reaction of H 2 O 2 and Fe(II) (i.e., Fenton chemistry). The temporal and spatial dynamics of H 2 O 2 and other dissolved compounds [Fe(II), Fe(III), H 2 S, O 2 ] were measured during a diel cycle (dark/light) in surface waters of three acidic geothermal springs (Beowulf Spring, One Hundred Springs Plain, and Echinus Geyser Spring; pH = 3-3.5, T = 68-80 • C) in Norris Geyser Basin, Yellowstone National Park. In situ analyses showed that H 2 O 2 concentrations were lowest (ca. 1 µM) in geothermal source waters containing high dissolved sulfide (and where oxygen was below detection) and increased by 2-fold (ca. 2-3 µM) in oxygenated waters corresponding to Fe(III)-oxide mat formation down the water channel. Small increases in dissolved oxygen and H 2 O 2 were observed during peak photon flux, but not consistently across all springs sampled. Iron-oxide microbial mats were sampled for molecular analysis of ROS gene expression in two primary autotrophs of acidic Fe(III)-oxide mat ecosystems: Metallosphaera yellowstonensis (Archaea) and Hydrogenobaculum sp. (Bacteria). Expression (RT-qPCR) assays of specific stress-response genes (e.g., superoxide dismutase, peroxidases) of the primary autotrophs were used to evaluate possible changes in transcription across temporal, spatial, and/or seasonal samples. Data presented here documented the presence of H 2 O 2 and general correlation with dissolved oxygen. Moreover, two dominant microbial populations expressed ROS response genes throughout the day, but showed less expression of key genes during peak sunlight. Oxidative stress response genes (especially external peroxidases) were highly-expressed in microorganisms within Fe(III)-oxide mat communities, suggesting a significant role for these proteins during survival and growth in situ.
“…High temperatures (480C), low pH (pHo3) conditions generally favor Archaea-dominated communities (Bolduc et al, 2012). Bacteria and eukaryotes are few or in many cases, absent (Reysenbach et al, 1994;Blank et al, 2002;Kozubal et al, 2012;Macur et al, 2012;Jay et al, 2013). These extreme environmental conditions favor not only the Archaea but also result in a relatively simplified microbial community structure.…”
Understanding of viral assemblage structure in natural environments remains a daunting task. Total viral assemblage sequencing (for example, viral metagenomics) provides a tractable approach. However, even with the availability of next-generation sequencing technology it is usually only possible to obtain a fragmented view of viral assemblages in natural ecosystems. In this study, we applied a network-based approach in combination with viral metagenomics to investigate viral assemblage structure in the high temperature, acidic hot springs of Yellowstone National Park, USA. Our results show that this approach can identify distinct viral groups and provide insights into the viral assemblage structure. We identified 110 viral groups in the hot springs environment, with each viral group likely representing a viral family at the sub-family taxonomic level. Most of these viral groups are previously unknown DNA viruses likely infecting archaeal hosts. Overall, this study demonstrates the utility of combining viral assemblage sequencing approaches with network analysis to gain insights into viral assemblage structure in natural ecosystems.
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