A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust

Abstract

Subsurface microbial communities comprise a significant fraction of the global prokaryotic biomass; however, the carbon metabolisms that support the deep biosphere have been relatively unexplored. In order to determine the predominant carbon metabolisms within a 3-km deep fracture fluid system accessed via the Tau Tona gold mine (Witwatersrand Basin, South Africa), metagenomic and thermodynamic analyses were combined. Within our system of study, the energy-conserving reductive acetyl-CoA (Wood-Ljungdahl) pathway was found to be the most abundant carbon fixation pathway identified in the metagenome. Carbon monoxide dehydrogenase genes that have the potential to participate in (1) both autotrophic and heterotrophic metabolisms through the reversible oxidization of CO and subsequent transfer of electrons for sulfate reduction, (2) direct utilization of H 2 and (3) methanogenesis were identified. The most abundant members of the metagenome belonged to Euryarchaeota (22%) and Firmicutes (57%)-by far, the highest relative abundance of Euryarchaeota yet reported from deep fracture fluids in South Africa and one of only five Firmicutes-dominated deep fracture fluids identified in the region. Importantly, by combining the metagenomics data and thermodynamic modeling of this study with previously published isotopic and community composition data from the South African subsurface, we are able to demonstrate that Firmicutes-dominated communities are associated with a particular hydrogeologic environment, specifically the older, more saline and more reducing waters.

Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea

“…Interestingly, YNP_45 and YNP_N21 have near-complete CBB pathways, only lacking two CBB genes: phosphoribulokinase ( prk) and fructose-1,6-bisphosphatase II ( glpX). The ability to fix inorganic carbon opens up a new source of carbon in the deep subsurface, where dissolved organic carbon has been shown to be extremely low 14,15 but inorganic carbon is readily available 16 .…”

“…It is therefore likely to occur widely in sediments and the subsurface. It has been estimated that after sulphate reduction, CO oxidation is the most energetically favourable anaerobic reaction in the deep terrestrial subsurface 15 . In addition to carbon monoxide (cox) genes, the YNP_45 Hadesarchaea bin also has distinct genes for catalytic nickel-containing CO dehydrogenase (CooS) and the iron sulphur subunits (CooF), suggesting that they are able to oxidize CO and H 2 O to CO 2 and H 2 as an energy source.…”

An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers

“…Methanogens and sulfate reducers, and the respective energy processes, are thought to be the dominant players and have been the research foci. Recent investigations showed that, in some deep, fluid-filled fractures in the Witwatersrand Basin, South Africa, methanogens contribute <5% of the total DNA and appear to produce sufficient CH 4 to support the rest of the diverse community. This paradoxical situation reflects our lack of knowledge about the in situ metabolic diversity and the overall ecological trophic structure of SLiMEs.…”

“…Whereas heterotrophs use dissolved organic carbon (DOC) transported from the surface and/or produced in situ, detrital organic deposits buried along with the sediments, and hydrocarbons migrating into petroleum reservoirs, chemolithoautotrophs fix dissolved inorganic carbon (DIC). In oligotrophic systems, subsurface lithoautotrophic microbial ecosystems (SLiMEs) (1) that are fueled by H 2 support the occurrence of autotrophic methanogens, acetogens, and sulfate reducers (2)(3)(4)(5). These environments can host highly diverse communities, consisting mostly of prokaryotes, but also multicellular microeukaryotes and viral particles (6)(7)(8)(9)(10)(11)(12)(13).…”

Tepidibacillus infernus sp. nov., a moderately thermophilic, selenate- and arsenate-respiring hydrolytic bacterium isolated from a gold mine, and emended description of the genus Tepidibacillus

“…However, scientific knowledge of these micro-organisms remains very limited due to the difficulties in accessing these environments and our inability to isolate the indigenous microbiota through traditional cultivation techniques (Colwell & D'Hondt, 2013). Molecular ecology studies of deep subsurface habitats have revealed the presence of micro-organisms of nearly all currently identified bacterial and archaeal phyla, both cultivated and uncultivated (candidate divisions) (Takai et al, 2001;Inagaki et al, 2003;Gihring et al, 2006), and recent studies have suggested that Firmicutes and Proteobacteria are the predominant phyla in many subterranean communities (Itavaara et al, 2011;Blanco et al, 2014;Magnabosco et al, 2016). Here we describe a novel species of phylum Firmicutes-Tepidibacillus infernus strain MBL-TLP T , isolated from a microbial mat sample of a 3540-m-deep layer of the TauTona gold mine, one of the deepest mines in the world.…”