Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade

Marshall, Katharine T.; Morris, Robert M.

doi:10.1038/ismej.2012.78

Cited by 114 publications

(119 citation statements)

References 18 publications

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“…If these organisms are able to utilise substrates of vent origin at relatively low temperatures and low concentrations, then entrainment effectively primes the plume with the nearbottom community ready for growth. A potential example of this in nature is the gammaproteobacterium SUP05, which is found in diffuse flow regimes yet also thrives in hydrothermal plumes (Huber et al, 2003;Sunamura et al, 2004;Anderson et al, 2012;Lesniewski et al, 2012;Marshall and Morris, 2013). At the uppermost point of the modelled rising plume, the ratio of vent fluid to ambient seawater is on the order of 1:10 4 , consistent with observations (for example, Lupton et al, 1985).…”

Section: Resultssupporting

confidence: 62%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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Submarine hydrothermal vents perturb the deep-ocean microbiome by injecting reduced chemical species into the water column that act as an energy source for chemosynthetic organisms. These systems thus provide excellent natural laboratories for studying the response of microbial communities to shifts in marine geochemistry. The present study explores the processes that regulate coupled microbial-geochemical dynamics in hydrothermal plumes by means of a novel mathematical model, which combines thermodynamics, growth and reaction kinetics, and transport processes derived from a fluid dynamics model. Simulations of a plume located in the ABE vent field of the Lau basin were able to reproduce metagenomic observations well and demonstrated that the magnitude of primary production and rate of autotrophic growth are largely regulated by the energetics of metabolisms and the availability of electron donors, as opposed to kinetic parameters. Ambient seawater was the dominant source of microbes to the plume and sulphur oxidisers constituted almost 90% of the modelled community in the neutrally-buoyant plume. Data from drifters deployed in the region allowed the different time scales of metabolisms to be cast in a spatial context, which demonstrated spatial succession in the microbial community. While growth was shown to occur over distances of tens of kilometers, microbes persisted over hundreds of kilometers. Given that high-temperature hydrothermal systems are found less than 100 km apart on average, plumes may act as important vectors between different vent fields and other environments that are hospitable to similar organisms, such as oil spills and oxygen minimum zones.

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Section: Resultssupporting

confidence: 62%

Section: Introductionmentioning

confidence: 99%

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

et al. 2015

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“…2). Absence of soxCD genes in SUP05 populations may result in storage of elemental sulfur and provisioning of SUP05 with an electron donor (25), similar to the recently cultivated heterotrophic ARCTIC96BD-19 clade bacterium (26).…”

Section: Resultsmentioning

confidence: 87%

“…GB-2 also contains a single putative di/tri carboxylate transporter. The presence of these transporters is intriguing because it may suggest an alternative source of carbon and nitrogen and hint at a mixotrophic lifestyle with the ability to use organic carbon as in the recently cultivated and closely related ARCTIC96BD-19 clade bacteria (8,26). For the purpose of nitrogen assimilation and metabolism, GB-1 and -2 genomes have multiple copies of genes for ammonium transport and a full complement of assimilatory nitrite reduction genes for reduction of nitrite (NO 2 − ) to ammonia (NH 3 ).…”

Section: Resultsmentioning

confidence: 99%

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

Anantharaman¹,

Breier

Sheik³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

176

224

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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 ...

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“…GSO comprises two closely related subgroups: SUP05 and ARCTIC96BD-19 (Walsh et al, 2009). Although ARCTIC96BD-19 is widespread in the surface (Marshall and Morris, 2013) and deep ocean (Swan et al, 2011) Table S4). On the basis of spectral counts, transporters for amino acids were the most abundant.…”

Section: Metabolism Of the Arctic96bd-19 Cladementioning

confidence: 99%

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

et al. 2014

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In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.

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Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade

Cited by 114 publications

References 18 publications

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

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

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

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

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