Metabolic strategies shared by basement residents of the Lost City hydrothermal field

Abstract

Alkaline fluids venting from chimneys of the Lost City hydrothermal field flow from a potentially vast microbial habitat within the seafloor where energy and organic molecules are released by chemical reactions within rocks uplifted from Earth's mantle. In this study, we investigated hydrothermal fluids venting from Lost City chimneys as windows into subseafloor environments where the products of geochemical reactions, such as hydrogen (H2), formate, and methane, may be the only available sources of energy for biological activity. Our deep sequencing of metagenomes and metatranscriptomes from these hydrothermal fluids revealed a few key species of archaea and bacteria that are likely to play critical roles in the subseafloor microbial ecosystem. We identified a population of Thermodesulfovibrionales (belonging to phylum Nitrospirae) as a prevalent sulfate-reducing bacterium that may be responsible for much of the consumption of H2 and sulfate in Lost City fluids. Metagenome-assembled genomes (MAGs) classified as Methanosarcinaceae and Candidatus Bipolaricaulota were also recovered from venting fluids and represent potential methanogenic and acetogenic members of the subseafloor ecosystem. These genomes share novel hydrogenases and formate dehydrogenase-like sequences that may be unique to hydrothermal and subsurface alkaline environments where hydrogen and formate are much more abundant than carbon dioxide. The results of this study include multiple examples of metabolic strategies that appear to be advantageous in hydrothermal and subsurface environments where energy and carbon are provided by geochemical reactions.

Microbial ecology of a shallow alkaline hydrothermal vent: Strýtan Hydrothermal Field, Eyjafördur, northern Iceland

“…DNA was extracted from the Sterivex filter cartridges using a lab protocol previously developed for low-biomass alkaline fluid samples ( Brazelton et al, 2022 ). Briefly, cell lysis was performed by alternating freeze/thaw cycles in an alkaline buffer, followed by purification with phenol-chloroform and precipitation with ethanol.…”

“…We cross-referenced the taxa detected in previous studies of alkaline submarine vents ( Quéméneur et al, 2014 ; Postec et al, 2015 ; Lecoeuvre et al, 2021 ; Brazelton et al, 2022 ) and alkaline hot springs ( Reysenbach et al, 1994 ; Marteinsson et al, 2001a ; Blank et al, 2002 ; Nakagawa and Fukui, 2003 ; Purcell et al, 2007 ; Boomer et al, 2009 ; Meyer-Dombard et al, 2011 ; Tobler and Benning, 2011 ; Meyer-Dombard and Amend, 2014 ; López-López et al, 2015 ; Martinez et al, 2019 ) with the abundant (>1% of any sample) taxa detected in this study ( Supplementary Table 3 ). For studies conducted with clone-libraries, we included all reported taxa ( Reysenbach et al, 1994 ; Marteinsson et al, 2001a ; Blank et al, 2002 ; Nakagawa and Fukui, 2003 ; Purcell et al, 2007 ; Boomer et al, 2009 ; Meyer-Dombard et al, 2011 ; Tobler and Benning, 2011 ; Meyer-Dombard and Amend, 2014 ; Quéméneur et al, 2014 ; Postec et al, 2015 ), while for studies conducted with amplicon and/or metagenomic sequencing, we included taxa representing a relative abundance of >1% of any sample ( López-López et al, 2015 ; Martinez et al, 2019 ; Lecoeuvre et al, 2021 ; Brazelton et al, 2022 ). Similarities between phylum through genus for Archaeon and class through genus for Bacteria were included with the lowest common taxonomic level reported in Supplementary Table 3 .…”

“…Specifically, the geochemistry of these systems appears to provide a template for autotrophic metabolic pathways ( McCollom and Seewald, 2007 ; Proskurowski et al, 2008 ; Hudson et al, 2020 ), such as the Wood-Ljungdahl pathway shared by methanogens, acetogens, and sulfate-reducers ( Martin and Russell, 2007 ; Adam et al, 2018 ; Hudson et al, 2020 ), which may be one of the most ancient metabolic pathways ( Ward and Shih, 2019 ). Previous work on submarine alkaline hydrothermal vents has focused on systems fueled by serpentinization, such as Lost City ( Kelley et al, 2005 ; Lang and Brazelton, 2020 ; Brazelton et al, 2022 ), Prony ( Monnin et al, 2014 ; Quéméneur et al, 2014 ; Postec et al, 2015 ), and Old City hydrothermal fields ( Lecoeuvre et al, 2021 ). While incredibly valuable, these studies have left many open questions about how opportunities for microbial life may differ in alkaline hydrothermal vents with different geological bases.…”

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

“…Generation, assembly, and annotation of metagenomes from the Lost City Hydrothermal Field (LCHF) have been described previously (35), and are briefly summarized here. In 2018, the remotely operated vehicle (ROV) Jason collected samples of fluids venting from chimneys at the LCHF, which is located near the Mid-Atlantic Ridge at 30 ºN latitude and a depth of ~800 m.…”

A naturalist perspective of microbiology: Examples from methanogenic archaea

“…Chief among these is how early autotrophs would have originated in an environment undergoing active serpentinization, where dissolved inorganic carbon (DIC; ∑CO 2 /HCO 3 − /CO 3 2− ) is highly limiting due to hyperalkaline conditions that accompany serpentinization reactions. Studies of modern serpentinites emplaced on continents (i.e., ophiolites) recently showed methanogen inhabitants to be dependent on HCOO − and acetogens dependent on both HCOO − and possibly CO as electron donors and carbon sources (Brazelton et al, 2022; Colman et al, 2022; Fones et al, 2021). In the case of methanogens, it was suggested that the dependence on HCOO − allowed cells to overcome DIC limitation and enable methanogenic energy generation to proceed by generating cytoplasmic DIC via HCOO − oxidation (Fones et al, 2021).…”