Methane- and Sulfur-Metabolizing Microbial Communities Dominate the Lost City Hydrothermal Field Ecosystem

Abstract

Hydrothermal venting and the formation of carbonate chimneys in the Lost City hydrothermal field (LCHF) are driven predominantly by serpentinization reactions and cooling of mantle rocks, resulting in a highly reducing, high-pH environment with abundant dissolved hydrogen and methane. Phylogenetic and terminal restriction fragment length polymorphism analyses of 16S rRNA genes in fluids and carbonate material from this site indicate the presence of organisms similar to sulfur-oxidizing, sulfate-reducing, and methane-oxidizing Bacteria as well as methanogenic and anaerobic methane-oxidizing Archaea. The presence of these metabolic groups indicates that microbial cycling of sulfur and methane may be the dominant biogeochemical processes active within this ultramafic rock-hosted environment. 16S rRNA gene sequences grouping within the Methylobacter and Thiomicrospira clades were recovered from a chemically diverse suite of carbonate chimney and fluid samples. In contrast, 16S rRNA genes corresponding to the Lost City Methanosarcinales phylotype were found exclusively in high-temperature chimneys, while a phylotype of anaerobic methanotrophic Archaea (ANME-1) was restricted to lower-temperature, less vigorously venting sites. A hyperthermophilic habitat beneath the LCHF may be reflected by 16S rRNA gene sequences belonging to Thermococcales and uncultured Crenarchaeota identified in vent fluids. The finding of a diverse microbial ecosystem supported by the interaction of high-temperature, high-pH fluids resulting from serpentinization reactions in the subsurface provides insight into the biogeochemistry of what may be a pervasive process in ultramafic subseafloor environments.The Lost City hydrothermal field (LCHF) is located near the summit of the Atlantis Massif at a water depth of ϳ750 m (37, 38). Long-lived faulting and extensive uplift at the massif have resulted in the exposure of magnesium-rich, variably altered ultramafic rocks with lesser gabbroic material that is 1.5 to 2 million years of age. Fluid circulation within the massif is driven by serpentinization reactions and the cooling of the underlying mantle rocks. These reactions result in a combination of extreme conditions never before seen in the marine environment, which include venting of high-pH (from pH 9 to 11), 40 to 91°C hydrothermal fluids with high concentrations of dissolved hydrogen (H 2 ), methane (CH 4 ), and other lowmolecular-weight hydrocarbons (38). Mixing of the warm, high-pH fluids with seawater results in carbonate precipitation and growth of chimneys, which tower up to 60 m above the surrounding seafloor (38). Carbon-14 radioisotopic dating indicates that hydrothermal activity has been ongoing for at least 30,000 years (17). A large percentage of exposed seafloor on and near slow-and ultraslow-spreading ridges is likely to contain ultramafic rocks similar to those that host the LCHF (4, 12, 14). Therefore, this system offers a unique opportunity to study an ultramafic-rock-hosted submarine ecosystem that may be both widespread and ...

A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

“…Our findings can explain the previously puzzling high abundance of Thiomicrospira species in sulfide-poor but hydrogen-rich hydrothermal habitats (Lost City) (Brazelton et al, 2006, Brazelton andBaross, 2010;. They can also explain the hydrogen consumption measured in incubations with Lilliput hydrothermal fluids, which were enriched with T. crunogena (28%) at the end of the experiments (Perner et al, 2011).…”

“…Phylogenetically diverse microorganisms can oxidize these reduced substrates whereby they gain energy that some can use for autotrophic CO 2 fixation (Campbell et al, 2006, Jannasch and Mottl, 1985, Miroshnichenko and Bonch-Osmolovskaya, 2006. If Thiomicrospira indeed cannot utilize hydrogen in habitats like Lost City, where sulfide is particularly scarce, but hydrogen is highly abundant, the widespread predominance of Thiomicrospira is somewhat puzzling (Brazelton et al, 2006Brazelton and Baross, 2010).…”

Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm

“…Abundant transposases in a hydrothermal biofilm WJ Brazelton and JA Baross 5-8 Â coverage), indicating that they represent the genome of a Thiomicrospira species that previous studies have shown to be widespread in Lost City carbonate chimneys (Brazelton et al, 2006). The 689 contigs containing transposases, by contrast, have a wide range in their %GC, and many have high sequence coverage and are less than 5 kb (Figure 2).…”

“…Previous studies have highlighted the extremely low microbial diversity in carbonate chimneys. Although a single phylotype belonging to the Methanosarcinales order of methane-cycling archaea constitutes 480% of all active cells in the hottest, anoxic zones of the chimney (Schrenk et al, 2004), a few species of aerobic and microaerophilic bacteria dominate the cooler, oxygenated zones (Brazelton et al, 2006). As the continuous mixing of anoxic hydrothermal fluid with oxygenated seawater creates micro-scale redox gradients within the chimneys, these anaerobic archaea and aerobic bacteria live in close proximity to each other.…”

Abundance and distribution of fatty acids within the walls of an active deep-sea sulfide chimney

“…The sulfur-based metabolic process is one of the most important metabolism approaches in the hydrothermal environment (Corre et al, 2001;Brazelton et al, 2006). Compared with the concentration in the surrounding ambient seawater, high temperature hydrothermal fluids contain concentrations of hydrogen sulfide several orders of magnitude higher (Ding et al, 2001), which is one of the best substrates for the chemolithoautotrophic bacteria in the hydrothermal environment (McCollom and Shock, 1997;Van Dover, 2000;Levin and Michener, 2002).…”