Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types

Amend, Jan P.; McCollom, T. M.; Hentscher, Michael; Bach, Wolfgang

doi:10.1016/j.gca.2011.07.041

Cited by 191 publications

(189 citation statements)

References 78 publications

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“…Results presented here suggest that energy availability shapes microbial communities that inhabit hydrothermal systems, in agreement with previous studies (for example, Shock et al, 1995;McCollom and Shock, 1997;McCollom, 2000McCollom, , 2007Amend et al, 2011;Boettger et al, 2013;Nakamura and Takai, 2014). Nevertheless, while this principle may be accurate in a broad sense, observations that do not conform to this paradigm hint at unresolved mechanisms and additional complexities.…”

Section: Resultssupporting

confidence: 92%

“…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.…”

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: 92%

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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“…Further, these results indicate that H 2 oxidation can account for up to 22% of the energy budget of SUP05 in warmer fluids of rising hydrothermal plumes (3.0-5.9°C), which have not yet been studied from a microbiological perspective. This prominent role for H 2 oxidation is consistent with previous studies that have modeled available energy in hydrothermal plumes (15); H 2 oxidation is expected to play an even more important role in ultramafic-hosted hydrothermal systems (37). Among sulfur species, we found S 0 oxidation with both oxygen and nitrate to be thermodynamically favored relative to H 2 S, thiosulfate, and particulate metal sulfides.…”

Section: Thermodynamic Model For Estimation Of Plume Chemistry Andsupporting

confidence: 91%

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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“…In Situ Biomass Production Thermodynamic predictions provide valuable constraints on possible metabolic (catabolic and anabolic) reactions in hydrothermal mixing zones. Amend et al (41) calculated that hydrogen oxidation in peridotite-hosted hydrothermal systems yields the most catabolic energy at low to moderate temperatures (<∼45°C) and seawater : hydrothermal fluid mixing ratios of >10. Other aerobic and anaerobic reactions, including methane oxidation, sulfate reduction, and methanogenesis, are exergonic under these conditions but, energetically, less favorable than hydrogen oxidation.…”

Section: Carbon Geochemistry Of a Suboceanic Mixing Zonementioning

confidence: 99%

“…Other aerobic and anaerobic reactions, including methane oxidation, sulfate reduction, and methanogenesis, are exergonic under these conditions but, energetically, less favorable than hydrogen oxidation. Similar to catabolic reactions, anabolic reactions are most favorable at high seawater : hydrothermal fluid mixing ratios and temperatures ≤ 32°C in peridotite-hosted hydrothermal systems with energy yields of ∼900 J per gram of dry cell mass (41). Assuming serpentinization fluids beneath the Iberia Abyssal Plain had a temperature of ∼150-250°C as indicated from oxygen isotope thermometry, and bottom seawater was ∼2°C, we calculate isenthalpic seawater : hydrothermal fluid mixing ratios of ∼3-15 to yield carbonate precipitation temperatures of 20-40°C.…”

Section: Carbon Geochemistry Of a Suboceanic Mixing Zonementioning

confidence: 99%

Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin

Klein

Humphris

Guo

et al. 2015

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

100

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Subseafloor mixing of reduced hydrothermal fluids with seawater is believed to provide the energy and substrates needed to support deep chemolithoautotrophic life in the hydrated oceanic mantle (i.e., serpentinite). However, geosphere-biosphere interactions in serpentinite-hosted subseafloor mixing zones remain poorly constrained. Here we examine fossil microbial communities and fluid mixing processes in the subseafloor of a Cretaceous Lost City-type hydrothermal system at the magma-poor passive Iberia Margin (Ocean Drilling Program Leg 149, Hole 897D). Brucite−calcite mineral assemblages precipitated from mixed fluids ca. 65 m below the Cretaceous paleo-seafloor at temperatures of 31.7 ± 4.3°C within steep chemical gradients between weathered, carbonate-rich serpentinite breccia and serpentinite. Mixing of oxidized seawater and strongly reducing hydrothermal fluid at moderate temperatures created conditions capable of supporting microbial activity. Dense microbial colonies are fossilized in brucite−calcite veins that are strongly enriched in organic carbon (up to 0.5 wt.% of the total carbon) but depleted in 13 C (δ 13 C TOC = −19.4‰). We detected a combination of bacterial diether lipid biomarkers, archaeol, and archaeal tetraethers analogous to those found in carbonate chimneys at the active Lost City hydrothermal field. The exposure of mantle rocks to seawater during the breakup of Pangaea fueled chemolithoautotrophic microbial communities at the Iberia Margin, possibly before the onset of seafloor spreading. Lost City-type serpentinization systems have been discovered at midocean ridges, in forearc settings of subduction zones, and at continental margins. It appears that, wherever they occur, they can support microbial life, even in deep subseafloor environments.serpentinization | microfossils | lipid biomarkers | brucite−calcite | passive margin

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Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types

Cited by 191 publications

References 78 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

Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin

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