Fractionation of sulfur isotopes by continuous cultures of <i>Desulfovibrio desulfuricans</i>

Chambers, L. A.; Trudinger, P. A.; Smith, J. W.; Burns, M.S.

doi:10.1139/m75-234

Cited by 175 publications

(129 citation statements)

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“…Under pure-culture laboratory conditions, this sulfi de can be depleted by up to 40‰-45‰ relative to the sulfate (Chambers et al, 1975;Canfi eld, 2001;Detmers et al, 2001). Instantaneous fractionations of this magnitude are observed during BSR even at very low initial sulfate concentrations ranging down to 200 μM, or less than 1% of the concentration in modern seawater.…”

Section: Sulfur Isotopesmentioning

confidence: 97%

Proterozoic sedimentary exhalative (SEDEX) deposits and links to evolving global ocean chemistry

Lyons¹,

Gellatly²,

McGoldrick³

et al. 2006

Evolution of Early Earth's Atmosphere, Hydrosphere, and Biosphere - Constraints From Ore Deposits

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Sedimentary exhalative (SEDEX) Zn-Pb-sulfi de mineralization fi rst occurred on a large scale during the late Paleoproterozoic. Metal sulfi des in most Proterozoic deposits have yielded broad ranges of predominantly positive δ 34 S values traditionally attributed to bacterial sulfate reduction. Heavy isotopic signatures are often ascribed to fractionation within closed or partly closed local reservoirs isolated from the global ocean by rifting before, during, and after the formation of Rodinia. Although such conditions likely played a central role, we argue here that the fi rst appearance of signifi cant SEDEX mineralization during the Proterozoic and the isotopic properties of those deposits are also strongly coupled to temporal evolution of the amount of sulfate in seawater.The ubiquity of 34 S-enriched sulfi de in ore bodies and shales and the widespread stratigraphic patterns of rapid δ 34 S variability expressed in both sulfate and sulfi de data are among the principal evidence for global seawater sulfate that was increasing during the Proterozoic but remained substantially lower than today. Because sulfate is produced mostly through weathering of the continents in the presence of oxygen, low Proterozoic concentrations imply that levels of atmospheric oxygen fell between the abundances of the Phanerozoic and the defi ciencies of the Archean, which are also indicated by the Precambrian sulfur isotope record. Given the limited availability of atmospheric oxygen, deep-water anoxia may have persisted well into the Proterozoic in the presence of a growing sulfate reservoir, which promoted prevalent euxinia. Collectively, these observations suggest that the mid-Proterozoic maximum in SEDEX mineralization and the absence of Archean deposits refl ect a critical threshold in the accumulation of oceanic sulfate and thus sulfi de within anoxic bottom waters and pore fl uids-conditions that favored both the production and preservation of sulfi de mineralization at or just below the seafl oor. Consistent with these evolving global conditions, the appearance of voluminous SEDEX mineralization ca. 1800 Ma coincides generally with the disappearance of banded iron formations-marking the transition from an early iron-dominated ocean to one more strongly infl uenced by sulfi de availability. 170 T.W. Lyons et al.

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Section: Sulfur Isotopesmentioning

confidence: 97%

Proterozoic sedimentary exhalative (SEDEX) deposits and links to evolving global ocean chemistry

Lyons¹,

Gellatly²,

McGoldrick³

et al. 2006

Evolution of Early Earth's Atmosphere, Hydrosphere, and Biosphere - Constraints From Ore Deposits

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“…The kinetic isotopic enrichment, ε 34 S, deduced from trends in the ␦ 34 S values of SO 4 2Ϫ and HS Ϫ in batch culture microbial SO 4 2Ϫ reduction experiments using the Rayleigh relationship, ranges from Ϫ2‰ to Ϫ46‰ (6,7,11,17,22,27,28,30,31,38,39). The variation in ε 34 S values has been attributed to the SO 4 2Ϫ concentration, the type of electron donor and its concentration, the SO 4 2Ϫ reduction rate per cell (csSRR) (22), temperature, and species-specific isotope enrichment effects.…”

Section: Dissimilatory Somentioning

confidence: 99%

“…SO 4 2Ϫ reduction is a dominant pathway for organic degradation in marine sediments (23) and in terrestrial subsurface settings where sulfur-bearing minerals dominate over Fe 3ϩ -bearing minerals. For example, at depths greater than 1.5 km below land surface in the fractured sedimentary and igneous rocks of the Witwatersrand Basin of South Africa, SO 4 2Ϫ reduction is the dominant electron-accepting process (3,26,46,48,61).The enrichment of S pyrite and ␦ 34 S barite/gypsum are the isotopic compositions of pyrite and barite or gypsum) increases from Ϫ10‰ in the 3.47-billion-year-old North Pole deposits to Ϫ30‰ in late-Archaean deposits (55), to Ϫ75‰ in Neoproterozoic to modern sulfide-bearing marine sediments (13).The kinetic isotopic enrichment, ε 34 S, deduced from trends in the ␦ 34 S values of SO 4 2Ϫ and HS Ϫ in batch culture microbial SO 4 2Ϫ reduction experiments using the Rayleigh relationship, ranges from Ϫ2‰ to Ϫ46‰ (6,7,11,17,22,27,28,30,31,38,39). The variation in ε 34 S values has been attributed to the SO 4 2Ϫ concentration, the type of electron donor and its concentration, the SO 4 2Ϫ reduction rate per cell (csSRR) (22), temperature, and species-specific isotope enrichment effects.…”

mentioning

confidence: 99%

Sulfur Isotope Enrichment during Maintenance Metabolism in the Thermophilic Sulfate-Reducing Bacterium Desulfotomaculum putei

Davidson

Bisher

Pratt

et al. 2009

Appl Environ Microbiol

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Values of ⌬ 34S SO4 indicate the differences in the isotopic compositions of the HS ؊ and SO 4 2؊ in the eluent, respectively) for many modern marine sediments are in the range of ؊55 to ؊75‰, much greater than the ؊2 to ؊46‰ 34 S (kinetic isotope enrichment) values commonly observed for microbial sulfate reduction in laboratory batch culture and chemostat experiments. It has been proposed that at extremely low sulfate reduction rates under hypersulfidic conditions with a nonlimited supply of sulfate, isotopic enrichment in laboratory culture experiments should increase to the levels recorded in nature. We examined the effect of extremely low sulfate reduction rates and electron donor limitation on S isotope fractionation by culturing a thermophilic, sulfate-reducing bacterium, Desulfotomaculum putei, in a biomass-recycling culture vessel, or "retentostat." The cell-specific rate of sulfate reduction and the specific growth rate decreased progressively from the exponential phase to the maintenance phase, yielding average maintenance coefficients of 10 ؊16 to 10 ؊18 mol of SO 4 cell ؊1 h ؊1 toward the end of the experiments. Overall S mass and isotopic balance were conserved during the experiment. The differences in the ␦ 34 S values of the sulfate and sulfide eluting from the retentostat were significantly larger, attaining a maximum ⌬ 34 S of ؊20.9‰, than the ؊9.7‰ observed during the batch culture experiment, but differences did not attain the values observed in marine sediments. Dissimilatory SO 42Ϫ reduction is a geologically ancient, anaerobic, energy-yielding metabolic process during which SO 4 2Ϫ -reducing bacteria (SRB) reduce SO 4 2Ϫ to H 2 S while oxidizing organic molecules or H 2 . SO 4 2Ϫ reduction is a dominant pathway for organic degradation in marine sediments (23) and in terrestrial subsurface settings where sulfur-bearing minerals dominate over Fe 3ϩ -bearing minerals. For example, at depths greater than 1.5 km below land surface in the fractured sedimentary and igneous rocks of the Witwatersrand Basin of South Africa, SO 4 2Ϫ reduction is the dominant electron-accepting process (3,26,46,48,61).The enrichment of S pyrite and ␦ 34 S barite/gypsum are the isotopic compositions of pyrite and barite or gypsum) increases from Ϫ10‰ in the 3.47-billion-year-old North Pole deposits to Ϫ30‰ in late-Archaean deposits (55), to Ϫ75‰ in Neoproterozoic to modern sulfide-bearing marine sediments (13).The kinetic isotopic enrichment, ε 34 S, deduced from trends in the ␦ 34 S values of SO 4 2Ϫ and HS Ϫ in batch culture microbial SO 4 2Ϫ reduction experiments using the Rayleigh relationship, ranges from Ϫ2‰ to Ϫ46‰ (6,7,11,17,22,27,28,30,31,38,39). The variation in ε 34 S values has been attributed to the SO 4 2Ϫ concentration, the type of electron donor and its concentration, the SO 4 2Ϫ reduction rate per cell (csSRR) (22), temperature, and species-specific isotope enrichment effects. In these laboratory experiments, doubling times are on the order of hours and csSRRs range from to 0.1 to 18 fmol cell Ϫ1 h Ϫ1 ...

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“…At high concentrations of sulfate, it is the rate of respiration of sulfate within a microbial cell that appears to explain a large portion of the isotopic selectivity. Increasing csSRR is observed to affect the magnitude of S isotope fractionation in a hyperbolically decreasing manner (8)(9)(10)(11)(12)(13)(14). This behavior likely results from the enhanced production of respiratory enzymes with increasing csSRR, which leads to diminished isotopic sensitivity to csSRR (5).…”

mentioning

confidence: 94%

“…If growth and, in turn, the energy supplied by sulfate respiration influence survival, then the controls on sulfate uptake, the internal regulation of concentrations of metabolites, and the structure of enzymes involved in the sulfate-reducing pathway could be key selective targets that influence the isotope phenotype (5). Previous work has emphasized exclusively physiological and environmental controls on the S isotope phenotype, including temperature, sulfate concentrations, and the nature and supply rate of the electron donor (1,(6)(7)(8)(9)(10)(11)(12)(13)(14). Among these controls, cell-specific sulfate respiration rate (csSRR) has emerged as a sort of master variable that sets the physiological level of S isotope fractionation.…”

mentioning

confidence: 99%

Sulfur Isotope Fractionation during the Evolutionary Adaptation of a Sulfate-Reducing Bacterium

Pellerin

Anderson-Trocmé

Whyte

et al. 2015

Appl Environ Microbiol

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c Dissimilatory sulfate reduction is a microbial catabolic pathway that preferentially processes less massive sulfur isotopes relative to their heavier counterparts. This sulfur isotope fractionation is recorded in ancient sedimentary rocks and generally is considered to reflect a phenotypic response to environmental variations rather than to evolutionary adaptation. Modern sulfate-reducing microorganisms isolated from similar environments can exhibit a wide range of sulfur isotope fractionations, suggesting that adaptive processes influence the sulfur isotope phenotype. To date, the relationship between evolutionary adaptation and isotopic phenotypes has not been explored. We addressed this by studying the covariation of fitness, sulfur isotope fractionation, and growth characteristics in Desulfovibrio vulgaris Hildenborough in a microbial evolution experiment. After 560 generations, the mean fitness of the evolved lineages relative to the starting isogenic population had increased by ϳ17%. After 927 generations, the mean fitness relative to the initial ancestral population had increased by ϳ20%. Growth rate in exponential phase increased during the course of the experiment, suggesting that this was a primary influence behind the fitness increases. Consistent changes were observed within different selection intervals between fractionation and fitness. Fitness changes were associated with changes in exponential growth rate but changes in fractionation were not. Instead, they appeared to be a response to changes in the parameters that govern growth rate: yield and cell-specific sulfate respiration rate. We hypothesize that cell-specific sulfate respiration rate, in particular, provides a bridge that allows physiological controls on fractionation to cross over to the adaptive realm. Dissimilatory sulfate reduction (DSR) is a microbial metabolism that consumes sulfate and utilizes this sulfur as a terminal electron acceptor, excreting sulfide. This process creates characteristic enrichments and depletions in the stable isotopes of sulfur that are preserved in sediments and sedimentary rocks as a legacy of the metabolic processing (1). In this way, sulfur isotope fractionation can be thought of as a phenotypic trait of the specific microbes that perform DSR. When the rock record is examined like this, the S isotope phenotype has been interpreted to be continually present in ancient sediments back to at least Ϸ3.5 billion years ago (2). However, the interpretation of S isotope fractionation as a phenotypic trait that can be preserved in ancient rocks opens up a basic question: does evolutionary adaptation influence the S isotope phenotype?Evolution-driven modifications to lineages of sulfate reducers (3, 4) may be capable of influencing the isotope phenotype by modifying the relative processing rates within the DSR pathway. If growth and, in turn, the energy supplied by sulfate respiration influence survival, then the controls on sulfate uptake, the internal regulation of concentrations of metabolites, and the struct...

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Fractionation of sulfur isotopes by continuous cultures of Desulfovibrio desulfuricans

Abstract: Sulfur isotope effects observed in lactate-limited continuous cultures of Desulfovibrio desulfuricans were, in general, similar to those reported for sulfate reduction by washed cells and batch cultures. There was a trend towards higher fractionation at low growth rates.

Cited by 175 publications

References 0 publications

Proterozoic sedimentary exhalative (SEDEX) deposits and links to evolving global ocean chemistry

Proterozoic sedimentary exhalative (SEDEX) deposits and links to evolving global ocean chemistry

Sulfur Isotope Enrichment during Maintenance Metabolism in the Thermophilic Sulfate-Reducing Bacterium Desulfotomaculum putei

Sulfur Isotope Fractionation during the Evolutionary Adaptation of a Sulfate-Reducing Bacterium

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