Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent

Perner, Mirjam; Petersen, Jillian M.; Zielinski, Frank; Gennerich, Hans‐Hermann; Seifert, Richard

doi:10.1111/j.1574-6941.2010.00940.x

Cited by 37 publications

(28 citation statements)

References 77 publications

(133 reference statements)

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“…For every measurement 1 ml of the headspace was taken, diluted 1:87 and from this dilution 2 ml injected into the GC. Hydrogen consumption rates were calculated as described before (Perner et al, 2010). Cell numbers were determined by direct cell counting using a counting chamber (Hawksley, Sussex, UK).…”

Section: In Vivo Hydrogen Consumption Experimentsmentioning

confidence: 99%

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A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

Hansen

Perner

2014

The ISME Journal

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Thiomicrospira species are ubiquitously found in various marine environments and appear particularly common in hydrothermal vent systems. Members of this lineage are commonly classified as sulfur-oxidizing chemolithoautotrophs. Although sequencing of Thiomicrospira crunogena's genome has revealed genes that encode enzymes for hydrogen uptake activity and for hydrogenase maturation and assembly, hydrogen uptake ability has so far not been reported for any Thiomicrospira species. We isolated a Thiomicrospira species (SP-41) from a deep sea hydrothermal vent and demonstrated that it can oxidize hydrogen. We show in vivo hydrogen consumption, hydrogen uptake activity in partially purified protein extracts and transcript abundance of hydrogenases during different growth stages. The ability of this strain to oxidize hydrogen opens up new perspectives with respect to the physiology of Thiomicrospira species that have been detected in hydrothermal vents and that have so far been exclusively associated with sulfur oxidation.

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Section: In Vivo Hydrogen Consumption Experimentsmentioning

confidence: 99%

“…16S rRNA and hynL gene sequences were edited and analyzed as previously described (Perner et al, 2009;. Phylogenetic trees were calculated using PhyML (Guindon and Gascuel, 2003) and settings as described before (Perner et al, 2009(Perner et al, , 2010.…”

Section: Fluorescence In Situ Hybridizationmentioning

confidence: 99%

A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

Hansen

Perner

2014

The ISME Journal

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“…Some of these studies have noted possible relationships between the metabolic abundances and compositions of hydrothermal vent-endemic microbial communities and the chemical characteristics of hydrothermal vent fluids in deep-sea hydrothermal systems (Perner et al 2007(Perner et al , 2010; Reysenbach and Shock 2002;Takai and Horikoshi 1999;Takai et al 2001Takai et al , 2004a. However, most of these studies were qualitative and focused mainly on the genetic and phylogenetic diversity of microbial communities and their constituents.…”

Section: Introductionmentioning

confidence: 99%

Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems

Nakamura

Takai

2014

Prog Earth Planet Sci

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In the past few decades, chemosynthetic ecosystems at deep-sea hydrothermal vents have received attention as plausible analogues to the early ecosystems of Earth, as well as to extraterrestrial ecosystems. These ecosystems are sustained by chemical energy obtained from inorganic redox substances (e.g., H 2 S, CO 2 , H 2 , CH 4 , and O 2 ) in hydrothermal fluids and ambient seawater. The chemical and isotope compositions of the hydrothermal fluid are, in turn, controlled by subseafloor physical and chemical processes, including fluid-rock interactions, phase separation and partitioning of fluids, and precipitation of minerals. We hypothesized that specific physicochemical principles describe the linkages among the living ecosystems, hydrothermal fluids, and geological background in deep-sea hydrothermal systems. We estimated the metabolic energy potentially available for productivity by chemolithotrophic microorganisms at various hydrothermal vent fields. We used a geochemical model based on hydrothermal fluid chemistry data compiled from 89 globally distributed hydrothermal vent sites. The model estimates were compared to the observed variability in extant microbial communities in seafloor hydrothermal environments. Our calculations clearly show that representative chemolithotrophic metabolisms (e.g., thiotrophic, hydrogenotrophic, and methanotrophic) respond differently to geological and geochemical variations in the hydrothermal systems. Nearly all of the deep-sea hydrothermal systems provide abundant energy for organisms with aerobic thiotrophic metabolisms; observed variations in the H 2 S concentrations among the hydrothermal fluids had little effect on the energetics of thiotrophic metabolism. Thus, these organisms form the base of the chemosynthetic microbial community in global deep-sea hydrothermal environments. In contrast, variations in H 2 concentrations in hydrothermal fluids significantly impact organisms with aerobic and anaerobic hydrogenotrophic metabolisms. Particularly in H 2 -rich ultramafic rock-hosted hydrothermal systems, anaerobic and aerobic hydrogenotrophy is more energetically significant than thiotrophy. The CH 4 concentration also has a considerable impact on organisms with aerobic and anaerobic methanotrophic metabolisms, particularly in sediment-associated hydrothermal systems. Recently clarified patterns and functions of existing microbial communities and their metabolisms are generally consistent with the results of our thermodynamic modeling of the hydrothermal mixing zones. These relationships provide important directions for future research addressing the origin and early evolution of life on Earth as well as for the search for extraterrestrial life.

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“…Previous studies incubating vent fluids at both in situ temperature and pressure are, to our knowledge, limited to an experiment conducted by Wirsen et al (1986). Therefore, this study greatly expands the range of data and can be used for comparison of rates to recent studies that were not carried out at in situ pressure (Bourbonnais et al, 2012;Perner et al, 2010Perner et al, , 2011Perner et al, , 2013.…”

Section: Rates Of Chemosynthetic Processes At In Situ Pressure and Tementioning

confidence: 90%

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

McNichol¹

2016

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Chemoautotrophic ecosystems at deep-sea hydrothermal vents were discovered in 1977, but not until 1995 were free-living autotrophic Epsilonproteobacteria identified as important microbial community members. Because the deep-sea is food-starved, the autotrophic metabolism of hydrothermal vent Epsilonproteobacteria may be very important for deep-sea consumers. However, quantifying their metabolic activities in situ has remained difficult, and biochemical mechanisms underlying their autotrophic physiology are poorly described. To gain insight into environmental processes, an approach was developed for incubations of microbes at in situ pressure and temperature (25 MPa, 24 o C) with various combinations of electron donors/acceptors (H 2 , O 2 and NO 3 -and 13 HCO 3 -) as a tracer to track carbon fixation. During short (18-24 h) incubations of low-temperature vent fluids from Crab Spa (9 o N East Pacific Rise), the concentration of electron donors/acceptors and cell numbers were monitored to quantify microbial processes. Measured rates were generally higher than previous studies, and the stoichiometry of microbially-catalyzed redox reactions revealed new insights into sulfur and nitrogen cycling. Single-cell, taxonomically-resolved tracer incorporation showed Epsilonproteobacteria dominated carbon fixation, and their growth efficiency was calculated based on electron acceptor consumption. Using these data, in situ primary productivity, microbial standing stock, and average biomass residence time of the deep-sea vent subseafloor biosphere were estimated. Finally, the population structures of the most abundant genera Sulfurimonas and Thioreductor were shown to be strongly influenced by pO 2 and temperature respectively, providing a mechanism for niche differentiation in situ. To gain insights into the core biochemical reactions underlying autotrophy in Epsilonprotebacteria, a theoretical metabolic model of Sulfurimonas denitrificans was developed. Validated iteratively by comparing in silico yields with data from chemostat experiments, the model generated hypotheses explaining critical, yet so far unresolved reactions supporting chemoautotrophy in Epsilonproteobacteria. For example, it provides insight into how energy is conserved during sulfur oxidation coupled to denitrification, how reverse electron transport produces ferredoxin for carbon fixation, and why aerobic growth yields are only slightly higher compared to denitrification. As a whole, this thesis provides important contributions towards understanding core mechanisms of chemoautrophy, as well as the in situ productivity, physiology and ecology of autotrophic Epsilonproteobacteria.

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Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent

Cited by 37 publications

References 77 publications

A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

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