Genomic Evidence for Formate Metabolism by Chloroflexi as the Key to Unlocking Deep Carbon in Lost City Microbial Ecosystems

Abstract

The Lost City hydrothermal field on the Mid-Atlantic Ridge supports dense microbial life on the lofty calcium carbonate chimney structures. The vent field is fueled by chemical reactions between the ultramafic rock under the chimneys and ambient seawater. These serpentinization reactions provide reducing power (as hydrogen gas) and organic compounds that can serve as microbial food; the most abundant of these are methane and formate. Previous studies have characterized the interior of the chimneys as a single-species biofilm inhabited by the Lost City Methanosarcinales, but they also indicated that this methanogen is unable to metabolize formate. The new metagenomic results presented here indicate that carbon cycling in these Lost City chimney biofilms could depend on the metabolism of formate by Chloroflexi populations. Additionally, we present evidence for metabolically diverse, formate-utilizing Sulfurovum populations and new genomic and phylogenetic insights into the unique Lost City Methanosarcinales. IMPORTANCE Primitive forms of life may have originated around hydrothermal vents at the bottom of the ancient ocean. The Lost City hydrothermal vent field, fueled by just rock and water, provides an analog for not only primitive ecosystems but also potential extraterrestrial rock-powered ecosystems. The microscopic life covering the towering chimney structures at the Lost City has been previously documented, yet little is known about the carbon cycling in this ecosystem. These results provide a better understanding of how carbon from the deep subsurface can fuel rich microbial ecosystems on the seafloor.

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

“…4 ), two sites characterized by strongly reducing conditions where these phylotypes are also abundant [ 13 , 14 , 19 ]. Moreover, [NiFe]-hydrogenase-encoding genes were also detected in reconstructed genomes of LCHF Chloroflexi [ 68 ]. These [NiFe]-hydrogenases-encoding genes are also found in OCHF Alpha- and Gammaproteobacteria (Fig.…”

Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif

“…The microbial genera identified in the shallow subsurface of the Atlantis Massif by amplicon sequencing were distinct from those described previously from LCHF fluids and chimneys, which are dominated by methane-oxidizing Methylomonas , sulfate-reducing Thiomicrospira , and the archaeal methanogens and methanotrophs Methanosarcinales and ANME-1 ( 20 , 21 , 23 ). This indicates that endolithic communities in the shallow subsurface of the Atlantis Massif are distinct from those in the actively venting LCHF system.…”

“…These by-products can be used by microorganisms for carbon and energy in the subsurface. For example, LCHF vent fluids have large amounts of methane, supporting low diversity, methane-cycling Archaea , sulfur-oxidizing Bacteria , and formate utilization ( 16 , 19 – 23 ). While the LCHF represents a unique, high-pH microbial community, the nature of the biosphere within the crustal core of the Atlantis Massif is unknown.…”

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)

“…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. Such an hypothesize has been recently formulated to tentatively explain the metabolism of the Lost City Methanosarcinales (LCMS), unable to use abiotically produced formate as dissolved carbon source, and thus would be dependent of anaerobic formate-oxidizing bacteria, present in the same micro-niche, feeding them with CO2 [67,68].…”