Metabolic Strategies Shared by Basement Residents of the Lost City Hydrothermal Field

Brazelton, William J.; McGonigle, Julia M.; Motamedi, Shahrzad; Pendleton, H. Lizethe; Twing, Katrina I.; Miller, Briggs C.; Lowe, W. J.; Hoffman, Alessandrina M.; Prator, Cecilia A.; Chadwick, Grayson L.; Anderson, R.; Butterfield, D. A.; Aquino, Karmina A.; Früh-Green, Gretchen L.; Schrenk, M. O.; Lang, Susan Q.

doi:10.1128/aem.00929-22

Cited by 23 publications

(50 citation statements)

References 124 publications

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“…For the pangenomic analysis, the MAGs to compare against our study were downloaded from public databases deposited as a part of research efforts (Takami et al, 2012;Jungbluth et al, 2017;Parks et al, 2017;Hao et al, 2018;Kadnikov et al, 2019;Smith et al, 2019;Youssef et al, 2019;Liu et al, 2020;Reysenbach et al, 2020;Zhou et al, 2020;Bhattarai et al, 2021;Schneider et al, 2021;Wang et al, 2021;Brazelton et al, 2022;Speth et al, 2022). Supplementary Table 2 provides information on the 23 origins of all the genomes examined in this study.…”

Section: Metagenomic Analysismentioning

confidence: 99%

Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey

Coskun

Gomez‐Saez²,

Beren³

et al. 2023

Front. Microbiol.

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Terrestrial hydrothermal springs and aquifers are excellent sites to study microbial biogeography because of their high physicochemical heterogeneity across relatively limited geographic regions. In this study, we performed 16S rRNA gene sequencing and metagenomic analyses of the microbial diversity of 11 different geothermal aquifers and springs across the tectonically active Biga Peninsula (Turkey). Across geothermal settings ranging in temperature from 43 to 79°C, one of the most highly represented groups in both 16S rRNA gene and metagenomic datasets was affiliated with the uncultivated phylum “Candidatus Bipolaricaulota” (former “Ca. Acetothermia” and OP1 division). The highest relative abundance of “Ca. Bipolaricaulota” was observed in a 68°C geothermal brine sediment, where it dominated the microbial community, representing 91% of all detectable 16S rRNA genes. Correlation analysis of “Ca. Bipolaricaulota” operational taxonomic units (OTUs) with physicochemical parameters indicated that salinity was the strongest environmental factor measured associated with the distribution of this novel group in geothermal fluids. Correspondingly, analysis of 23 metagenome-assembled genomes (MAGs) revealed two distinct groups of “Ca. Bipolaricaulota” MAGs based on the differences in carbon metabolism: one group encoding the bacterial Wood-Ljungdahl pathway (WLP) for H2 dependent CO2 fixation is selected for at lower salinities, and a second heterotrophic clade that lacks the WLP that was selected for under hypersaline conditions in the geothermal brine sediment. In conclusion, our results highlight that the biogeography of “Ca. Bipolaricaulota” taxa is strongly correlated with salinity in hydrothermal ecosystems, which coincides with key differences in carbon acquisition strategies. The exceptionally high relative abundance of apparently heterotrophic representatives of this novel candidate Phylum in geothermal brine sediment observed here may help to guide future enrichment experiments to obtain representatives in pure culture.

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Section: Metagenomic Analysismentioning

confidence: 99%

Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey

Coskun

Gomez‐Saez²,

Beren³

et al. 2023

Front. Microbiol.

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“…Another explanation for the source of OG in basement microbes of the LCHF, which is suggested by our gene inventory analysis (Table 2 and Supporting Information), involves reactive sulfur species (RSS) and reactive nitrogen species (RNS). Many of the basementdwelling microbes within the LCHF appear to metabolize sulfur and nitrogen for energy conservation (4,36), strategies that generate RSS and RNS as metabolic byproducts (67,68).…”

Section: Discussionmentioning

confidence: 99%

“…The environmental distributions of MutY-encoding MAGs were inspected for potential signs of contamination from ambient seawater during sample collection. This possibility was ruled out by the absence of all MutY-encoding taxa reported in this study in the background seawater samples collected by Brazelton et al (36). MAG completeness and contamination scores were generated by CheckM v1.0.5 as described in Brazelton et al 2022 (36).…”

Section: Taxonomic Classificationmentioning

confidence: 94%

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Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal Field

Utzman

Mays

Miller

et al. 2023

Preprint

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The GO DNA repair system protects against GC → TC mutations by finding and removing oxidized guanine. The system is mechanistically well understood but its origins are unknown. We searched metagenomes and abundantly found the genes encoding GO DNA repair at the Lost City Hydrothermal Field (LCHF). We recombinantly expressed the final enzyme in the system to show MutY homologs function to suppress mutations. Microbes at the LCHF thrive without sunlight, fueled by the products of geochemical transformations of seafloor rocks, under conditions believed to resemble a young Earth. High levels of the reductant H2 and low levels of O2 in this environment raise the question, why are resident microbes equipped to repair damage caused by oxidative stress? MutY genes could be assigned to metagenome assembled genomes (MAGs), and thereby associate GO DNA repair with metabolic pathways that generate reactive oxygen, nitrogen and sulfur species. Our results indicate that cell-based life was under evolutionary pressure to cope with oxidized guanine well before O2 levels rose following the great oxidation event.

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“…In high-temperature anoxic environments, H 2 is generally considered to be the primary electron donor and CO 2 the primary carbon source for autotrophic metabolism. However, recently other electron donors and carbon sources such as formate have been considered as alternatives ( Windman et al, 2007 ), especially in high pH environments where dissolved inorganic carbon precipitates as calcium carbonate and is largely unavailable to autotrophs ( Lang et al, 2018 ; McGonigle et al, 2020 ; Brazelton et al, 2022 ). There are strong links between formate and H 2 in hydrothermal environments and in the physiology of microbes that consume and produce formate and H 2 .…”

Section: Introductionmentioning

confidence: 99%

Formate and hydrogen in hydrothermal vents and their use by extremely thermophilic methanogens and heterotrophs

Holden

Sistu

2023

Front. Microbiol.

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Extremely thermophilic methanogens in the Methanococci and heterotrophs in the Thermococci are common in deep-sea hydrothermal vents. All Methanococci use H2 as an electron donor, and a few species can also use formate. Most Methanococci have a coenzyme F420-reducing formate dehydrogenase. All Thermococci reduce S0 but have hydrogenases and produce H2 in the absence of S0. Some Thermococci have formate hydrogenlyase (Fhl) that reversibly converts H2 and CO2 to formate or an NAD(P)+-reducing formate dehydrogenase (Nfd). Questions remain if Methanococci or Thermococci use or produce formate in nature, why only certain species can grow on or produce formate, and what the physiological role of formate is? Formate forms abiotically in hydrothermal fluids through chemical equilibrium with primarily H2, CO2, and CO and is strongly dependent upon H2 concentration, pH, and temperature. Formate concentrations are highest in hydrothermal fluids where H2 concentrations are also high, such as in ultramafic systems where serpentinization reactions occur. In nature, Methanococci are likely to use formate as an electron donor when H2 is limiting. Thermococci with Fhl likely convert H2 and CO2 to formate when H2 concentrations become inhibitory for growth. They are unlikely to grow on formate in nature unless formate is more abundant than H2 in the environment. Nearly all Methanococci and Thermococci have a gene for at least one formate dehydrogenase catalytic subunit, which may be used to provide free formate for de novo purine biosynthesis. However, only species with a membrane-bound formate transporter can grow on or secrete formate. Interspecies H2 transfer occurs between Thermococci and Methanococci. This and putative interspecies formate transfer may support Methanococci in low H2 environments, which in turn may prevent growth inhibition of Thermococci by its own H2. Future research directions include understanding when, where, and how formate is used and produced by these organisms in nature, and how transcription of Thermococci genes encoding formate-related enzymes are regulated.

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Metabolic Strategies Shared by Basement Residents of the Lost City Hydrothermal Field

Cited by 23 publications

References 124 publications

Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey

Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey

Metagenome mining and functional analysis reveal oxidized guanine DNA repair at the Lost City Hydrothermal Field

Formate and hydrogen in hydrothermal vents and their use by extremely thermophilic methanogens and heterotrophs

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