Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

Abstract

Hydrothermal vents are a well-known source of energy that powers chemosynthesis in the deep sea. Recent work suggests that microbial chemosynthesis is also surprisingly pervasive throughout the dark oceans, serving as a significant CO 2 sink even at sites far removed from vents. Ammonia and sulfur have been identified as potential electron donors for this chemosynthesis, but they do not fully account for measured rates of dark primary production in the pelagic water column. Here we use metagenomic and metatranscriptomic analyses to show that deep-sea populations of the SUP05 group of uncultured sulfur-oxidizing Gammaproteobacteria, which are abundant in widespread and diverse marine environments, contain and highly express genes encoding group 1 Ni, Fe hydrogenase enzymes for H 2 oxidation. Reconstruction of near-complete genomes of two cooccurring SUP05 populations in hydrothermal plumes and deep waters of the Gulf of California enabled detailed population-specific metatranscriptomic analyses, revealing dynamic patterns of gene content and transcript abundance. SUP05 transcripts for genes involved in H 2 and sulfur oxidation are most abundant in hydrothermal plumes where these electron donors are enriched. In contrast, a second hydrogenase has more abundant transcripts in background deep-sea samples. Coupled with results from a bioenergetic model that suggest that H 2 oxidation can contribute significantly to the SUP05 energy budget, these findings reveal the potential importance of H 2 as a key energy source in the deep ocean. This study also highlights the genomic plasticity of SUP05, which enables this widely distributed group to optimize its energy metabolism (electron donor and acceptor) to local geochemical conditions. Guaymas | oxygen minimum zone D eep-sea hydrothermal vent ecosystems depend on microorganisms that use reduced chemicals such as sulfur, methane, ammonium, and H 2 as electron donors for chemosynthesis (1-5). Recent work suggests that microbial chemosynthesis is also far more prevalent in the broader deep oceans than previously recognized, extending throughout the water column of the dark open ocean, where it serves as a significant source of organic carbon (6, 7). The fuels for this pelagic primary production remain unknown, but recent studies show that ammonium (3) and sulfur (8, 9) are potential electron donors in the water column. H 2 , long known as an energy source for free-living bacteria in seafloor hydrothermal systems, was also recently identified as an electron donor in hydrothermal vent animal symbioses (4). Although microbial communities at seafloor hydrothermal vent sites have attracted much attention, hydrothermal vent plumes remain poorly characterized despite their importance as habitats for free-living chemolithoautotrophs (10). These plume microorganisms mediate the hydrothermal transfer of elements from the lithosphere to the oceans (11, 12) and contribute significantly to organic carbon in the deep oceans via carbon fixation (1, 13-15).We investigated hydrothermal vent ...

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

“…Metagenomic analysis of SUP05 indicates the potential for a chemolithoautotrophic metabolism using sulfur compounds coupled to either aerobic respiration (Anantharaman et al, 2013) or denitrification (Walsh et al, 2009). Here, we identified SUP05 proteins for the sulfur oxidation pathway (SoxAB), the reverse dissimilatory sulfite reductase (DsrABCEK) and adenosine phosphosulfate reductase (Table 1).…”

“…Heterotrophic marine microbes exhibit various levels of specialization for the uptake and processing of specific components of the dissolved organic matter pool (Pomeroy et al, 2007;Poretsky et al, 2010;Teeling et al, 2012). Moreover, recent studies have uncovered novel metabolic capabilities in marine bacteria and archaea, including rhodopsin-based phototrophy (Béjà et al, 2000), aerobic anoxygenic phototrophy (Béjà et al, 2002), CO 2 fixation (Newton et al, 2010) and chemolithotrophic oxidation of inorganic compounds such as ammonia (Walker et al, 2010), sulfur (Walsh et al, 2009) and hydrogen (Anantharaman et al, 2013). Metagenomics and single-cell amplified genomes have provided insight into the diversity and metabolic potential of microbial communities in the ocean (DeLong et al, 2006;Yooseph et al, 2007;Woyke et al, 2009;Swan et al, 2011;Grzymski et al, 2012;Rinke et al, 2013).…”

Predicting the response of the deep-ocean microbiome to geochemical perturbations by hydrothermal vents

“…Expanding upon the suite of metabolisms used above, aerobic hydrogen oxidation was added to the model (that is, the 'Knallgas' reaction, H 2 þ ½O 2 -H 2 O), as this has been identified as a potentially important pathway in other hydrothermal systems (for example, McCollom, 2000McCollom, , 2007Anantharaman et al, 2013). Compared with those systems, however, fluid emanating from the ABE vent is somewhat depleted in H 2 (54-101 mmol kg À 1 ; Flores et al, 2012) suggesting that the relative abundance of hydrogenases-genes associated with hydrogen oxidation-should also be low.…”

“…Plumes may thus act as vectors, linking microbial communities in various marine environments . While recent metagenomic and metatranscriptomic studies have provided much-needed insight into those microbes present in plumes as well as their metabolisms (Baker et al, 2012;Lesniewski et al, 2012;Anantharaman et al, 2013;Baker et al, 2013;Marshall and Morris, 2013;Li et al, 2014;Sheik et al, in press), fundamental questions remain regarding the ecology and dynamics of these communities. Both near-vent and pelagic communities have been invoked as the origin of plume-dwelling microbes (Winn et al, 1986;Lesniewski et al, 2012), but how these potential sources interact with plume physics, vent chemistry and microbial growth to shape plume communities remains unclear.…”

“…Given that energy drives deep-sea autotrophy, thermodynamic mixing models have been used extensively over the past 20 years to estimate primary production in chimney walls, plumes and low-temperature diffuse flow regions of submarine hydrothermal systems (for example, Shock et al, 1995;McCollom and Shock, 1997;McCollom, 2000McCollom, , 2007Amend et al, 2011;Anantharaman et al, 2013;Boettger et al, 2013;Anantharaman et al, 2014;Nakamura and Takai, 2014). These models calculate the amount of energy that is potentially available through a wide range of pathways, thus predicting the prevalence of these metabolisms.…”