Microbial ecology of the newly discovered serpentinite-hosted Old City hydrothermal field (southwest Indian ridge)

Abstract

Lost City (mid-Atlantic ridge) is a unique oceanic hydrothermal field where carbonate-brucite chimneys are colonized by a single phylotype of archaeal Methanosarcinales, as well as sulfur- and methane-metabolizing bacteria. So far, only one submarine analog of Lost City has been characterized, the Prony Bay hydrothermal field (New Caledonia), which nonetheless shows more microbiological similarities with ecosystems associated with continental ophiolites. This study presents the microbial ecology of the ‘Lost City’-type Old City hydrothermal field, recently discovered along the southwest Indian ridge. Five carbonate-brucite chimneys were sampled and subjected to mineralogical and geochemical analyses, microimaging, as well as 16S rRNA-encoding gene and metagenomic sequencing. Dominant taxa and metabolisms vary between chimneys, in conjunction with the predicted redox state, while potential formate- and CO-metabolizing microorganisms as well as sulfur-metabolizing bacteria are always abundant. We hypothesize that the variable environmental conditions resulting from the slow and diffuse hydrothermal fluid discharge that currently characterizes Old City could lead to different microbial populations between chimneys that utilize CO and formate differently as carbon or electron sources. Old City discovery and this first description of its microbial ecology opens up attractive perspectives for understanding environmental factors shaping communities and metabolisms in oceanic serpentinite-hosted ecosystems.

Genomic evidence for a chemical link between redox conditions and microbial community composition

“…The main finding of this study is that the oxidation state of inferred community proteomes decreases in more reducing conditions at global and local scales. This conclusion is consistent with our earlier analysis of shotgun metagenomic data that showed lower Z C of proteins in Yellowstone hot springs compared to other environments (7) and a study from another group reporting that metagenome-encoded proteins for the newly discovered Old City hydrothermal field have lower Z C than ambient seawater (11) (the value for Z C of seawater communities used by (11) was taken from our previous study (7)). The present study also reveals decreasing Z C with depth using data from multiple studies for stratified water bodies; this strong physicochem-ical signal is in contrast to the ambiguous results for oxygen minimum zones that we previously obtained by analyzing shotgun metagenomic data (7).…”

“…Carbon oxidation state (Z C ) of an organic molecule denotes the average charge on carbon atoms required for electroneutrality given formal charges of all other atoms (9). Also known by other names such as nominal oxidation state of carbon, Z C is widely used in studies of natural organic matter, and to an increasing extent for comparing proteins coded by metagenomic sequences (10,11). The equation for Z C only requires elemental abundances (8,12) and is consistent with models for complex organic matter used, for example, in soil science (9).…”

“…Carbon oxidation state (Z C ) of an organic molecule denotes the average charge on carbon atoms required for electroneutrality given formal charges of all other atoms. Also known by other names such as nominal oxidation state of carbon (NOSC), Z C is an established metric for describing chemical transformations of natural organic matter (Kroll et al, 2011;Arndt et al, 2013;Visconti and de Paz, 2021), and has also been applied to analysis of metagenomic sequences (Fones et al, 2019;Lecoeuvre et al, 2021). The equation for Z C of proteins only requires elemental abundances (Dick, 2014;Dick et al, 2020).…”

Mid-Ocean Ridges and Their Geomorphological Features

“…Such systems have been identified to date along the Mid Atlantic Ridge (Lost City hydrothermal field; Kelley et al, 2005Denny et al, 2010, and the Southwest Indian Ridge (Lecoeuvre et al, 2021).…”

Alkaliphilus serpentinus sp. nov. and Alkaliphilus pronyensis sp. nov., two novel anaerobic alkaliphilic species isolated from the serpentinite-hosted Prony Bay Hydrothermal Field (New Caledonia)

“…The fermentative metabolism of PBHF Alkaliphilus lead to the production of H2 and organic acids (i.e., acetate, butyrate, propionate) in situ at concentrations that might sustain the growth of microbial partners in syntrophy. This hypothetical partners could be hydrogenotrophic autotrophs such as the elusive Methanosarcinales, that co-occur within the same chimney samples, or hypothetical homoacetogens such as the candidate phyla Bipolaricaulota (formely named Acetothermia) which are dominant in PBHF and LCHF [65] but also prevalent in terrestrial (ophiolites) serpentinized ecosystems [10,66]. Thus, the Methanosarcinales could benefit, not only of the H2 (also abiotically produced) but of the CO2, since the fluids are mostly depleted of DIC.…”