Evolution of electron transfer out of the cell

comparative genomics of six Geobacter genomes

Jessica E Butler, Nelson D Young, Derek R Lovley

Research output: Contribution to journalArticle

101 Citations (Scopus)
4 Downloads (Pure)

Abstract

BACKGROUND: Geobacter species grow by transferring electrons out of the cell--either to Fe(III)-oxides or to man-made substances like energy-harvesting electrodes. Study of Geobacter sulfurreducens has shown that TCA cycle enzymes, inner-membrane respiratory enzymes, and periplasmic and outer-membrane cytochromes are required. Here we present comparative analysis of six Geobacter genomes, including species from the clade that predominates in the subsurface. Conservation of proteins across the genomes was determined to better understand the evolution of Geobacter species and to create a metabolic model applicable to subsurface environments.

RESULTS: The results showed that enzymes for acetate transport and oxidation, and for proton transport across the inner membrane were well conserved. An NADH dehydrogenase, the ATP synthase, and several TCA cycle enzymes were among the best conserved in the genomes. However, most of the cytochromes required for Fe(III)-reduction were not, including many of the outer-membrane cytochromes. While conservation of cytochromes was poor, an abundance and diversity of cytochromes were found in every genome, with duplications apparent in several species.

CONCLUSIONS: These results indicate there is a common pathway for acetate oxidation and energy generation across the family and in the last common ancestor. They also suggest that while cytochromes are important for extracellular electron transport, the path of electrons across the periplasm and outer membrane is variable. This combination of abundant cytochromes with weak sequence conservation suggests they may not be specific terminal reductases, but rather may be important in their heme-bearing capacity, as sinks for electrons between the inner-membrane electron transport chain and the extracellular acceptor.

Original languageEnglish
Article number40
Number of pages12
JournalBMC Genomics
Volume11
DOIs
Publication statusPublished - 17 Jan 2010

Fingerprint

Geobacter
Cytochromes
Genomics
Genome
Electrons
Membranes
Enzymes
Electron Transport
Acetates
NADH Dehydrogenase
Periplasm
Heme
Oxides
Protons
Oxidoreductases
Electrodes
Adenosine Triphosphate

Keywords

  • acetates
  • bacterial proton-translocating ATPases
  • citric acid cycle
  • cluster analysis
  • comparative genomic hybridization
  • cytochromes c
  • electron transport
  • evolution, molecular
  • gene duplication
  • gene expression regulation, bacterial
  • gene transfer, horizontal
  • genome, bacterial
  • genomics
  • Geobacter
  • NADH dehydrogenase
  • oxidation-reduction
  • phylogeny

Cite this

Evolution of electron transfer out of the cell : comparative genomics of six Geobacter genomes. / Butler, Jessica E; Young, Nelson D; Lovley, Derek R.

In: BMC Genomics, Vol. 11, 40, 17.01.2010.

Research output: Contribution to journalArticle

@article{d09ecd4dd17f41db955519e657ec93c5,
title = "Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes",
abstract = "BACKGROUND: Geobacter species grow by transferring electrons out of the cell--either to Fe(III)-oxides or to man-made substances like energy-harvesting electrodes. Study of Geobacter sulfurreducens has shown that TCA cycle enzymes, inner-membrane respiratory enzymes, and periplasmic and outer-membrane cytochromes are required. Here we present comparative analysis of six Geobacter genomes, including species from the clade that predominates in the subsurface. Conservation of proteins across the genomes was determined to better understand the evolution of Geobacter species and to create a metabolic model applicable to subsurface environments.RESULTS: The results showed that enzymes for acetate transport and oxidation, and for proton transport across the inner membrane were well conserved. An NADH dehydrogenase, the ATP synthase, and several TCA cycle enzymes were among the best conserved in the genomes. However, most of the cytochromes required for Fe(III)-reduction were not, including many of the outer-membrane cytochromes. While conservation of cytochromes was poor, an abundance and diversity of cytochromes were found in every genome, with duplications apparent in several species.CONCLUSIONS: These results indicate there is a common pathway for acetate oxidation and energy generation across the family and in the last common ancestor. They also suggest that while cytochromes are important for extracellular electron transport, the path of electrons across the periplasm and outer membrane is variable. This combination of abundant cytochromes with weak sequence conservation suggests they may not be specific terminal reductases, but rather may be important in their heme-bearing capacity, as sinks for electrons between the inner-membrane electron transport chain and the extracellular acceptor.",
keywords = "acetates, bacterial proton-translocating ATPases, citric acid cycle, cluster analysis, comparative genomic hybridization, cytochromes c, electron transport, evolution, molecular, gene duplication, gene expression regulation, bacterial, gene transfer, horizontal, genome, bacterial, genomics, Geobacter, NADH dehydrogenase, oxidation-reduction, phylogeny",
author = "Butler, {Jessica E} and Young, {Nelson D} and Lovley, {Derek R}",
year = "2010",
month = "1",
day = "17",
doi = "10.1186/1471-2164-11-40",
language = "English",
volume = "11",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",

}

TY - JOUR

T1 - Evolution of electron transfer out of the cell

T2 - comparative genomics of six Geobacter genomes

AU - Butler, Jessica E

AU - Young, Nelson D

AU - Lovley, Derek R

PY - 2010/1/17

Y1 - 2010/1/17

N2 - BACKGROUND: Geobacter species grow by transferring electrons out of the cell--either to Fe(III)-oxides or to man-made substances like energy-harvesting electrodes. Study of Geobacter sulfurreducens has shown that TCA cycle enzymes, inner-membrane respiratory enzymes, and periplasmic and outer-membrane cytochromes are required. Here we present comparative analysis of six Geobacter genomes, including species from the clade that predominates in the subsurface. Conservation of proteins across the genomes was determined to better understand the evolution of Geobacter species and to create a metabolic model applicable to subsurface environments.RESULTS: The results showed that enzymes for acetate transport and oxidation, and for proton transport across the inner membrane were well conserved. An NADH dehydrogenase, the ATP synthase, and several TCA cycle enzymes were among the best conserved in the genomes. However, most of the cytochromes required for Fe(III)-reduction were not, including many of the outer-membrane cytochromes. While conservation of cytochromes was poor, an abundance and diversity of cytochromes were found in every genome, with duplications apparent in several species.CONCLUSIONS: These results indicate there is a common pathway for acetate oxidation and energy generation across the family and in the last common ancestor. They also suggest that while cytochromes are important for extracellular electron transport, the path of electrons across the periplasm and outer membrane is variable. This combination of abundant cytochromes with weak sequence conservation suggests they may not be specific terminal reductases, but rather may be important in their heme-bearing capacity, as sinks for electrons between the inner-membrane electron transport chain and the extracellular acceptor.

AB - BACKGROUND: Geobacter species grow by transferring electrons out of the cell--either to Fe(III)-oxides or to man-made substances like energy-harvesting electrodes. Study of Geobacter sulfurreducens has shown that TCA cycle enzymes, inner-membrane respiratory enzymes, and periplasmic and outer-membrane cytochromes are required. Here we present comparative analysis of six Geobacter genomes, including species from the clade that predominates in the subsurface. Conservation of proteins across the genomes was determined to better understand the evolution of Geobacter species and to create a metabolic model applicable to subsurface environments.RESULTS: The results showed that enzymes for acetate transport and oxidation, and for proton transport across the inner membrane were well conserved. An NADH dehydrogenase, the ATP synthase, and several TCA cycle enzymes were among the best conserved in the genomes. However, most of the cytochromes required for Fe(III)-reduction were not, including many of the outer-membrane cytochromes. While conservation of cytochromes was poor, an abundance and diversity of cytochromes were found in every genome, with duplications apparent in several species.CONCLUSIONS: These results indicate there is a common pathway for acetate oxidation and energy generation across the family and in the last common ancestor. They also suggest that while cytochromes are important for extracellular electron transport, the path of electrons across the periplasm and outer membrane is variable. This combination of abundant cytochromes with weak sequence conservation suggests they may not be specific terminal reductases, but rather may be important in their heme-bearing capacity, as sinks for electrons between the inner-membrane electron transport chain and the extracellular acceptor.

KW - acetates

KW - bacterial proton-translocating ATPases

KW - citric acid cycle

KW - cluster analysis

KW - comparative genomic hybridization

KW - cytochromes c

KW - electron transport

KW - evolution, molecular

KW - gene duplication

KW - gene expression regulation, bacterial

KW - gene transfer, horizontal

KW - genome, bacterial

KW - genomics

KW - Geobacter

KW - NADH dehydrogenase

KW - oxidation-reduction

KW - phylogeny

U2 - 10.1186/1471-2164-11-40

DO - 10.1186/1471-2164-11-40

M3 - Article

VL - 11

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

M1 - 40

ER -