Deconstructing the Dissimilatory Sulfate Reduction Pathway: Isotope Fractionation of a Mutant Unable of Growth on Sulfate

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Deconstructing the Dissimilatory Sulfate Reduction Pathway : Isotope Fractionation of a Mutant Unable of Growth on Sulfate. / Bertran, Emma; Leavitt, William D.; Pellerin, Andre; Zane, Grant M.; Wall, Judy D.; Halevy, Itay; Wing, Boswell A.; Johnston, David T.

In: Frontiers in Microbiology, Vol. 9, 3110, 14.12.2018.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

Harvard

Bertran, E, Leavitt, WD, Pellerin, A, Zane, GM, Wall, JD, Halevy, I, Wing, BA & Johnston, DT 2018, 'Deconstructing the Dissimilatory Sulfate Reduction Pathway: Isotope Fractionation of a Mutant Unable of Growth on Sulfate' Frontiers in Microbiology, vol. 9, 3110. https://doi.org/10.3389/fmicb.2018.03110

APA

Bertran, E., Leavitt, W. D., Pellerin, A., Zane, G. M., Wall, J. D., Halevy, I., ... Johnston, D. T. (2018). Deconstructing the Dissimilatory Sulfate Reduction Pathway: Isotope Fractionation of a Mutant Unable of Growth on Sulfate. Frontiers in Microbiology, 9, [3110]. https://doi.org/10.3389/fmicb.2018.03110

CBE

MLA

Vancouver

Author

Bertran, Emma ; Leavitt, William D. ; Pellerin, Andre ; Zane, Grant M. ; Wall, Judy D. ; Halevy, Itay ; Wing, Boswell A. ; Johnston, David T. / Deconstructing the Dissimilatory Sulfate Reduction Pathway : Isotope Fractionation of a Mutant Unable of Growth on Sulfate. In: Frontiers in Microbiology. 2018 ; Vol. 9.

Bibtex

@article{c66ff2d04c394a098b14e8d1a1ff41fa,
title = "Deconstructing the Dissimilatory Sulfate Reduction Pathway: Isotope Fractionation of a Mutant Unable of Growth on Sulfate",
abstract = "The sulfur isotope record provides key insight into the history of Earth's redox conditions. A detailed understanding of the metabolisms driving this cycle, and specifically microbial sulfate reduction (MSR), is crucial for accurate paleoenvironmental reconstructions. This includes a precise knowledge of the step-specific sulfur isotope effects during MSR. In this study, we aim at resolving the cellular-level fractionation factor during dissimilatory sulfite reduction to sulfide within MSR, and use this measured isotope effect as a calibration to enhance our understanding of the biochemistry of sulfite reduction. For this, we merge measured isotope effects associated with dissimilatory sulfite reduction with a quantitative model that explicitly links net fractionation, reaction reversibility, and intracellular metabolite levels. The highly targeted experimental aspect of this study was possible by virtue of the availability of a deletion mutant strain of the model sulfate reducer Desulfovibrio vulgaris (strain Hildenborough), in which the sulfite reduction step is isolated from the rest of the metabolic pathway owing to the absence of its QmoABC complex (Delta Qmo). This deletion disrupts electron flux and prevents the reduction of adenosine phosphosulfate (APS) to sulfite. When grown in open-system steady-state conditions at 10{\%} maximum growth rate in the presence of sulfite and lactate as electron donor, sulfur isotope fractionation factors averaged -15.9 parts per thousand (1 sigma = 0.4), which appeared to be statistically indistinguishable from a pure enzyme study with dissimilatory sulfite reductase. We coupled these measurements with an understanding of step-specific equilibrium and kinetic isotope effects, and furthered our mechanistic understanding of the biochemistry of sulfite uptake and ensuing reduction. Our metabolically informed isotope model identifies flavodoxin as the most likely electron carrier performing the transfer of electrons to dissimilatory sulfite reductase. This is in line with previous work on metabolic strategies adopted by sulfate reducers under different energy regimes, and has implications for our understanding of the plasticity of this metabolic pathway at the center of our interpretation of modern and palaeo-environmental records.",
keywords = "chemostat, deletion mutant, metabolic pathway, sulfite reduction, sulfur isotope fractionation, BACTERIAL REDUCTION, SULFUR ISOTOPES, BISULFITE ION, MODEL, BIOTURBATION, EVOLUTION, PROTEIN, MARINE",
author = "Emma Bertran and Leavitt, {William D.} and Andre Pellerin and Zane, {Grant M.} and Wall, {Judy D.} and Itay Halevy and Wing, {Boswell A.} and Johnston, {David T.}",
year = "2018",
month = "12",
day = "14",
doi = "10.3389/fmicb.2018.03110",
language = "English",
volume = "9",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A",

}

RIS

TY - JOUR

T1 - Deconstructing the Dissimilatory Sulfate Reduction Pathway

T2 - Isotope Fractionation of a Mutant Unable of Growth on Sulfate

AU - Bertran, Emma

AU - Leavitt, William D.

AU - Pellerin, Andre

AU - Zane, Grant M.

AU - Wall, Judy D.

AU - Halevy, Itay

AU - Wing, Boswell A.

AU - Johnston, David T.

PY - 2018/12/14

Y1 - 2018/12/14

N2 - The sulfur isotope record provides key insight into the history of Earth's redox conditions. A detailed understanding of the metabolisms driving this cycle, and specifically microbial sulfate reduction (MSR), is crucial for accurate paleoenvironmental reconstructions. This includes a precise knowledge of the step-specific sulfur isotope effects during MSR. In this study, we aim at resolving the cellular-level fractionation factor during dissimilatory sulfite reduction to sulfide within MSR, and use this measured isotope effect as a calibration to enhance our understanding of the biochemistry of sulfite reduction. For this, we merge measured isotope effects associated with dissimilatory sulfite reduction with a quantitative model that explicitly links net fractionation, reaction reversibility, and intracellular metabolite levels. The highly targeted experimental aspect of this study was possible by virtue of the availability of a deletion mutant strain of the model sulfate reducer Desulfovibrio vulgaris (strain Hildenborough), in which the sulfite reduction step is isolated from the rest of the metabolic pathway owing to the absence of its QmoABC complex (Delta Qmo). This deletion disrupts electron flux and prevents the reduction of adenosine phosphosulfate (APS) to sulfite. When grown in open-system steady-state conditions at 10% maximum growth rate in the presence of sulfite and lactate as electron donor, sulfur isotope fractionation factors averaged -15.9 parts per thousand (1 sigma = 0.4), which appeared to be statistically indistinguishable from a pure enzyme study with dissimilatory sulfite reductase. We coupled these measurements with an understanding of step-specific equilibrium and kinetic isotope effects, and furthered our mechanistic understanding of the biochemistry of sulfite uptake and ensuing reduction. Our metabolically informed isotope model identifies flavodoxin as the most likely electron carrier performing the transfer of electrons to dissimilatory sulfite reductase. This is in line with previous work on metabolic strategies adopted by sulfate reducers under different energy regimes, and has implications for our understanding of the plasticity of this metabolic pathway at the center of our interpretation of modern and palaeo-environmental records.

AB - The sulfur isotope record provides key insight into the history of Earth's redox conditions. A detailed understanding of the metabolisms driving this cycle, and specifically microbial sulfate reduction (MSR), is crucial for accurate paleoenvironmental reconstructions. This includes a precise knowledge of the step-specific sulfur isotope effects during MSR. In this study, we aim at resolving the cellular-level fractionation factor during dissimilatory sulfite reduction to sulfide within MSR, and use this measured isotope effect as a calibration to enhance our understanding of the biochemistry of sulfite reduction. For this, we merge measured isotope effects associated with dissimilatory sulfite reduction with a quantitative model that explicitly links net fractionation, reaction reversibility, and intracellular metabolite levels. The highly targeted experimental aspect of this study was possible by virtue of the availability of a deletion mutant strain of the model sulfate reducer Desulfovibrio vulgaris (strain Hildenborough), in which the sulfite reduction step is isolated from the rest of the metabolic pathway owing to the absence of its QmoABC complex (Delta Qmo). This deletion disrupts electron flux and prevents the reduction of adenosine phosphosulfate (APS) to sulfite. When grown in open-system steady-state conditions at 10% maximum growth rate in the presence of sulfite and lactate as electron donor, sulfur isotope fractionation factors averaged -15.9 parts per thousand (1 sigma = 0.4), which appeared to be statistically indistinguishable from a pure enzyme study with dissimilatory sulfite reductase. We coupled these measurements with an understanding of step-specific equilibrium and kinetic isotope effects, and furthered our mechanistic understanding of the biochemistry of sulfite uptake and ensuing reduction. Our metabolically informed isotope model identifies flavodoxin as the most likely electron carrier performing the transfer of electrons to dissimilatory sulfite reductase. This is in line with previous work on metabolic strategies adopted by sulfate reducers under different energy regimes, and has implications for our understanding of the plasticity of this metabolic pathway at the center of our interpretation of modern and palaeo-environmental records.

KW - chemostat

KW - deletion mutant

KW - metabolic pathway

KW - sulfite reduction

KW - sulfur isotope fractionation

KW - BACTERIAL REDUCTION

KW - SULFUR ISOTOPES

KW - BISULFITE ION

KW - MODEL

KW - BIOTURBATION

KW - EVOLUTION

KW - PROTEIN

KW - MARINE

U2 - 10.3389/fmicb.2018.03110

DO - 10.3389/fmicb.2018.03110

M3 - Journal article

VL - 9

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 3110

ER -