Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens

Evgenya S Shelobolina, Maddalena V Coppi, Anton A Korenevsky, Laurie N DiDonato, Sara A Sullivan, Hiromi Konishi, Huifang Xu, Ching Leang, Jessica E Butler, Byoung-Chan Kim, Derek R Lovley

Research output: Contribution to journalArticle

115 Citations (Scopus)

Abstract

BACKGROUND: In order to study the mechanism of U(VI) reduction, the effect of deleting c-type cytochrome genes on the capacity of Geobacter sulfurreducens to reduce U(VI) with acetate serving as the electron donor was investigated.

RESULTS: The ability of several c-type cytochrome deficient mutants to reduce U(VI) was lower than that of the wild type strain. Elimination of two confirmed outer membrane cytochromes and two putative outer membrane cytochromes significantly decreased (ca. 50-60%) the ability of G. sulfurreducens to reduce U(VI). Involvement in U(VI) reduction did not appear to be a general property of outer membrane cytochromes, as elimination of two other confirmed outer membrane cytochromes, OmcB and OmcC, had very little impact on U(VI) reduction. Among the periplasmic cytochromes, only MacA, proposed to transfer electrons from the inner membrane to the periplasm, appeared to play a significant role in U(VI) reduction. A subpopulation of both wild type and U(VI) reduction-impaired cells, 24-30%, accumulated amorphous uranium in the periplasm. Comparison of uranium-accumulating cells demonstrated a similar amount of periplasmic uranium accumulation in U(VI) reduction-impaired and wild type G. sulfurreducens. Assessment of the ability of the various suspensions to reduce Fe(III) revealed no correlation between the impact of cytochrome deletion on U(VI) reduction and reduction of Fe(III) hydroxide and chelated Fe(III).

CONCLUSION: This study indicates that c-type cytochromes are involved in U(VI) reduction by Geobacter sulfurreducens. The data provide new evidence for extracellular uranium reduction by G. sulfurreducens but do not rule out the possibility of periplasmic uranium reduction. Occurrence of U(VI) reduction at the cell surface is supported by the significant impact of elimination of outer membrane cytochromes on U(VI) reduction and the lack of correlation between periplasmic uranium accumulation and the capacity for uranium reduction. Periplasmic uranium accumulation may reflect the ability of uranium to penetrate the outer membrane rather than the occurrence of enzymatic U(VI) reduction. Elimination of cytochromes rarely had a similar impact on both Fe(III) and U(VI) reduction, suggesting that there are differences in the routes of electron transfer to U(VI) and Fe(III). Further studies are required to clarify the pathways leading to U(VI) reduction in G. sulfurreducens.

Original languageEnglish
Article number16
JournalBioMed Central Microbiology
Volume7
DOIs
Publication statusPublished - 8 Mar 2007

Fingerprint

Geobacter
Cytochrome c Group
Uranium
Cytochromes
Membranes
Periplasm
Electrons
Lepidium
Suspensions
Acetates

Keywords

  • Biodegradation, Environmental
  • Cytochrome c Group
  • Ferric Compounds
  • Geobacter
  • Microscopy, Electron, Transmission
  • Mutation
  • Oxidation-Reduction
  • Periplasm
  • Uranium

Cite this

Shelobolina, E. S., Coppi, M. V., Korenevsky, A. A., DiDonato, L. N., Sullivan, S. A., Konishi, H., ... Lovley, D. R. (2007). Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BioMed Central Microbiology, 7, [16]. https://doi.org/10.1186/1471-2180-7-16

Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. / Shelobolina, Evgenya S; Coppi, Maddalena V; Korenevsky, Anton A; DiDonato, Laurie N; Sullivan, Sara A; Konishi, Hiromi; Xu, Huifang; Leang, Ching; Butler, Jessica E; Kim, Byoung-Chan; Lovley, Derek R.

In: BioMed Central Microbiology, Vol. 7, 16, 08.03.2007.

Research output: Contribution to journalArticle

Shelobolina, ES, Coppi, MV, Korenevsky, AA, DiDonato, LN, Sullivan, SA, Konishi, H, Xu, H, Leang, C, Butler, JE, Kim, B-C & Lovley, DR 2007, 'Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens' BioMed Central Microbiology, vol. 7, 16. https://doi.org/10.1186/1471-2180-7-16
Shelobolina ES, Coppi MV, Korenevsky AA, DiDonato LN, Sullivan SA, Konishi H et al. Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BioMed Central Microbiology. 2007 Mar 8;7. 16. https://doi.org/10.1186/1471-2180-7-16
Shelobolina, Evgenya S ; Coppi, Maddalena V ; Korenevsky, Anton A ; DiDonato, Laurie N ; Sullivan, Sara A ; Konishi, Hiromi ; Xu, Huifang ; Leang, Ching ; Butler, Jessica E ; Kim, Byoung-Chan ; Lovley, Derek R. / Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens. In: BioMed Central Microbiology. 2007 ; Vol. 7.
@article{8848ef1a4478447583761c881286186f,
title = "Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens",
abstract = "BACKGROUND: In order to study the mechanism of U(VI) reduction, the effect of deleting c-type cytochrome genes on the capacity of Geobacter sulfurreducens to reduce U(VI) with acetate serving as the electron donor was investigated.RESULTS: The ability of several c-type cytochrome deficient mutants to reduce U(VI) was lower than that of the wild type strain. Elimination of two confirmed outer membrane cytochromes and two putative outer membrane cytochromes significantly decreased (ca. 50-60{\%}) the ability of G. sulfurreducens to reduce U(VI). Involvement in U(VI) reduction did not appear to be a general property of outer membrane cytochromes, as elimination of two other confirmed outer membrane cytochromes, OmcB and OmcC, had very little impact on U(VI) reduction. Among the periplasmic cytochromes, only MacA, proposed to transfer electrons from the inner membrane to the periplasm, appeared to play a significant role in U(VI) reduction. A subpopulation of both wild type and U(VI) reduction-impaired cells, 24-30{\%}, accumulated amorphous uranium in the periplasm. Comparison of uranium-accumulating cells demonstrated a similar amount of periplasmic uranium accumulation in U(VI) reduction-impaired and wild type G. sulfurreducens. Assessment of the ability of the various suspensions to reduce Fe(III) revealed no correlation between the impact of cytochrome deletion on U(VI) reduction and reduction of Fe(III) hydroxide and chelated Fe(III).CONCLUSION: This study indicates that c-type cytochromes are involved in U(VI) reduction by Geobacter sulfurreducens. The data provide new evidence for extracellular uranium reduction by G. sulfurreducens but do not rule out the possibility of periplasmic uranium reduction. Occurrence of U(VI) reduction at the cell surface is supported by the significant impact of elimination of outer membrane cytochromes on U(VI) reduction and the lack of correlation between periplasmic uranium accumulation and the capacity for uranium reduction. Periplasmic uranium accumulation may reflect the ability of uranium to penetrate the outer membrane rather than the occurrence of enzymatic U(VI) reduction. Elimination of cytochromes rarely had a similar impact on both Fe(III) and U(VI) reduction, suggesting that there are differences in the routes of electron transfer to U(VI) and Fe(III). Further studies are required to clarify the pathways leading to U(VI) reduction in G. sulfurreducens.",
keywords = "Biodegradation, Environmental, Cytochrome c Group, Ferric Compounds, Geobacter, Microscopy, Electron, Transmission, Mutation, Oxidation-Reduction, Periplasm, Uranium",
author = "Shelobolina, {Evgenya S} and Coppi, {Maddalena V} and Korenevsky, {Anton A} and DiDonato, {Laurie N} and Sullivan, {Sara A} and Hiromi Konishi and Huifang Xu and Ching Leang and Butler, {Jessica E} and Byoung-Chan Kim and Lovley, {Derek R}",
year = "2007",
month = "3",
day = "8",
doi = "10.1186/1471-2180-7-16",
language = "English",
volume = "7",
journal = "BioMed Central Microbiology",
issn = "1471-2180",
publisher = "BioMed Central",

}

TY - JOUR

T1 - Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens

AU - Shelobolina, Evgenya S

AU - Coppi, Maddalena V

AU - Korenevsky, Anton A

AU - DiDonato, Laurie N

AU - Sullivan, Sara A

AU - Konishi, Hiromi

AU - Xu, Huifang

AU - Leang, Ching

AU - Butler, Jessica E

AU - Kim, Byoung-Chan

AU - Lovley, Derek R

PY - 2007/3/8

Y1 - 2007/3/8

N2 - BACKGROUND: In order to study the mechanism of U(VI) reduction, the effect of deleting c-type cytochrome genes on the capacity of Geobacter sulfurreducens to reduce U(VI) with acetate serving as the electron donor was investigated.RESULTS: The ability of several c-type cytochrome deficient mutants to reduce U(VI) was lower than that of the wild type strain. Elimination of two confirmed outer membrane cytochromes and two putative outer membrane cytochromes significantly decreased (ca. 50-60%) the ability of G. sulfurreducens to reduce U(VI). Involvement in U(VI) reduction did not appear to be a general property of outer membrane cytochromes, as elimination of two other confirmed outer membrane cytochromes, OmcB and OmcC, had very little impact on U(VI) reduction. Among the periplasmic cytochromes, only MacA, proposed to transfer electrons from the inner membrane to the periplasm, appeared to play a significant role in U(VI) reduction. A subpopulation of both wild type and U(VI) reduction-impaired cells, 24-30%, accumulated amorphous uranium in the periplasm. Comparison of uranium-accumulating cells demonstrated a similar amount of periplasmic uranium accumulation in U(VI) reduction-impaired and wild type G. sulfurreducens. Assessment of the ability of the various suspensions to reduce Fe(III) revealed no correlation between the impact of cytochrome deletion on U(VI) reduction and reduction of Fe(III) hydroxide and chelated Fe(III).CONCLUSION: This study indicates that c-type cytochromes are involved in U(VI) reduction by Geobacter sulfurreducens. The data provide new evidence for extracellular uranium reduction by G. sulfurreducens but do not rule out the possibility of periplasmic uranium reduction. Occurrence of U(VI) reduction at the cell surface is supported by the significant impact of elimination of outer membrane cytochromes on U(VI) reduction and the lack of correlation between periplasmic uranium accumulation and the capacity for uranium reduction. Periplasmic uranium accumulation may reflect the ability of uranium to penetrate the outer membrane rather than the occurrence of enzymatic U(VI) reduction. Elimination of cytochromes rarely had a similar impact on both Fe(III) and U(VI) reduction, suggesting that there are differences in the routes of electron transfer to U(VI) and Fe(III). Further studies are required to clarify the pathways leading to U(VI) reduction in G. sulfurreducens.

AB - BACKGROUND: In order to study the mechanism of U(VI) reduction, the effect of deleting c-type cytochrome genes on the capacity of Geobacter sulfurreducens to reduce U(VI) with acetate serving as the electron donor was investigated.RESULTS: The ability of several c-type cytochrome deficient mutants to reduce U(VI) was lower than that of the wild type strain. Elimination of two confirmed outer membrane cytochromes and two putative outer membrane cytochromes significantly decreased (ca. 50-60%) the ability of G. sulfurreducens to reduce U(VI). Involvement in U(VI) reduction did not appear to be a general property of outer membrane cytochromes, as elimination of two other confirmed outer membrane cytochromes, OmcB and OmcC, had very little impact on U(VI) reduction. Among the periplasmic cytochromes, only MacA, proposed to transfer electrons from the inner membrane to the periplasm, appeared to play a significant role in U(VI) reduction. A subpopulation of both wild type and U(VI) reduction-impaired cells, 24-30%, accumulated amorphous uranium in the periplasm. Comparison of uranium-accumulating cells demonstrated a similar amount of periplasmic uranium accumulation in U(VI) reduction-impaired and wild type G. sulfurreducens. Assessment of the ability of the various suspensions to reduce Fe(III) revealed no correlation between the impact of cytochrome deletion on U(VI) reduction and reduction of Fe(III) hydroxide and chelated Fe(III).CONCLUSION: This study indicates that c-type cytochromes are involved in U(VI) reduction by Geobacter sulfurreducens. The data provide new evidence for extracellular uranium reduction by G. sulfurreducens but do not rule out the possibility of periplasmic uranium reduction. Occurrence of U(VI) reduction at the cell surface is supported by the significant impact of elimination of outer membrane cytochromes on U(VI) reduction and the lack of correlation between periplasmic uranium accumulation and the capacity for uranium reduction. Periplasmic uranium accumulation may reflect the ability of uranium to penetrate the outer membrane rather than the occurrence of enzymatic U(VI) reduction. Elimination of cytochromes rarely had a similar impact on both Fe(III) and U(VI) reduction, suggesting that there are differences in the routes of electron transfer to U(VI) and Fe(III). Further studies are required to clarify the pathways leading to U(VI) reduction in G. sulfurreducens.

KW - Biodegradation, Environmental

KW - Cytochrome c Group

KW - Ferric Compounds

KW - Geobacter

KW - Microscopy, Electron, Transmission

KW - Mutation

KW - Oxidation-Reduction

KW - Periplasm

KW - Uranium

U2 - 10.1186/1471-2180-7-16

DO - 10.1186/1471-2180-7-16

M3 - Article

VL - 7

JO - BioMed Central Microbiology

JF - BioMed Central Microbiology

SN - 1471-2180

M1 - 16

ER -