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Towards environmental systems biology of Shewanella

Nature Reviews Microbiology volume 6, pages 592–603 (2008)Cite this article

Key Points

  • Shewanella species couple the decomposition of organic matter to the reduction of various terminal electron acceptors that are present in the diverse environments that they can inhabit.

  • The metabolic versatility of Shewanella species makes them important mediators of carbon cycling, and allows for their potential use in the remediation of environments that are contaminated with radionuclides and other toxic metals, as well as potential sources of alternative energy through microbial fuel cells.

  • Systems-biology is being used to better understand the environmental sensing, signal-transduction and metabolic- and energy-generating pathways of the model organism Shewanella oneidensis MR-1.

  • Among other insights, this analysis has revealed the presence of novel metabolic pathways, the reorganization of regulatory pathways compared with Escherichia coli and other model organisms, and a novel mechanism for dealing with oxidative stress through autoaggregation.

  • Comparative genomic analysis, based on the availability of genome sequences for 23 Shewanella species, has facilitated the transfer of information gained from the study of S. oneidensis MR-1 across members of the genus.

  • Many of the proteins that are important for respiratory diversity in S. oneidensis MR-1 are conserved in many members of the genus.

Abstract

Bacteria of the genus Shewanella are known for their versatile electron-accepting capacities, which allow them to couple the decomposition of organic matter to the reduction of the various terminal electron acceptors that they encounter in their stratified environments. Owing to their diverse metabolic capabilities, shewanellae are important for carbon cycling and have considerable potential for the remediation of contaminated environments and use in microbial fuel cells. Systems-level analysis of the model species Shewanella oneidensis MR-1 and other members of this genus has provided new insights into the signal-transduction proteins, regulators, and metabolic and respiratory subsystems that govern the remarkable versatility of the shewanellae.

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Figure 1: Rewiring of transcriptional regulatory networks in the central carbon metabolism of Shewanella oneidensis MR-1.
Figure 2: Comparison of the metal-reductase-containing locus in Shewanella spp.
Figure 3: Five dimethyl sulphoxide (DMSO) family subsystems.

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Acknowledgements

The authors thank the numerous members of the Shewanella Federation for useful discussions and concepts during the course of their systems biology investigations of Shewanella, including E.J. Crane, H. Gao, C. Giometti, K. Kostantinidis, M. Lipton, M. Marshall, L.-A. McCue, A. Obraztsova, N. Samatova, H. Scholten, E. Uberbacher, L. Ulrich, M. Ward and J. Zhou. The authors have been supported by the US Department of Energy (DOE) through the Shewanella Federation consortium and by the National Science Foundation (grant number NSFMCB0543501).

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Authors and Affiliations

  1. Biological Sciences Division, Pacific Northwest National Laboratory, Richland, 99352, Washington, USA

    James K. Fredrickson, Margaret F. Romine, Alexander S. Beliaev & Grigoriy Pinchuk

  2. Center for Microbial Ecology, Michigan State University, East Lansing, Michigan, 48824, USA

    Jennifer M. Auchtung & James M. Tiedje

  3. Program in Bioinformatics, Boston University, Boston, 02215, Massachusetts, USA

    Michael E. Driscoll & Timothy S. Gardner

  4. Department of Earth Sciences, University of Southern California, Los Angeles, 90089, California, USA

    Kenneth H. Nealson

  5. Burnham Institute for Medical Research, La Jolla, 92037, California, USA

    Andrei L. Osterman & Dmitry A. Rodionov

  6. Department of Chemical and Biological Engineering, University of Wisconsin, Madison, 53706, Wisconsin, USA

    Jennifer L. Reed

  7. Department of Biology, University of Texas, Arlington, 76019, Texas, USA

    Jorge L. M. Rodrigues

  8. Department of Biological Sciences, University of Wisconsin, Milwaukee, 53211, Wisconsin, USA

    Daad A. Saffarini

  9. Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, 02543, Massachusetts, USA

    Margrethe H. Serres

  10. Departments of Biological Sciences, Chemical Engineering, Civil and Environmental Engineering, and Geological and Environmental Sciences, Stanford University, Stanford, 94305, California, USA

    Alfred M. Spormann

  11. Joint Institute for Computational Sciences, The University of Tennessee — Oak Ridge National Laboratory, Oak Ridge, 37831, Tennessee, USA

    Igor B. Zhulin

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Correspondence to James K. Fredrickson or James M. Tiedje.

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DATABASES

Entrez Genome Project

Dechloromonas aromatica

Escherichia coli

Geobacter uraniumreducens

Halorhodospira halophila

Magnetospirillum magneticum

Rhodopseudomonas palustris

Shewanella baltica

Shewanella denitrificans

Shewanella oneidensis MR-1

Shewanella woodyi

Vibrio splendidus

Entrez Protein

CymA

EtrA

FruR

MtrA

MtrB

MtrC

MtrF

NagC

OmcA

FURTHER INFORMATION

List of Prokaryotic names with Standing in Nomenclature

Glossary

Dissimilatory

An enzymatic reaction in which a compound is oxidized or reduced but is not assimilated or incorporated into cells for the purposes of biosynthesis during, for example, respiration.

Electron acceptor

An oxidant used during cellular respiration.

One-component system

A regulatory protein that combines both sensory and regulatory capabilities that usually reside in two distinct domains. The repressor of the lactose operons (LacI) and the catabolite activator protein of Escherichia coli are classical examples.

Two-component system

A regulatory system that is typically composed of two proteins, a sensor histidine kinase and a cognate response regulator. EnvZ and OmpR of Escherichia coli are classical examples.

PAS domain

A ubiquitous sensory domain that is found in many one-component and two-component regulatory systems in prokaryotes, as well as in regulatory proteins in eukaryotes. The PAS domain was named after three proteins that it was found in: Per (period circadian protein), Arnt (receptor nuclear translocator protein) and Sim (single-minded protein).

Diguanylate cyclase

An enzyme that synthesizes cyclic diguanylic acid and typically contains the canonical amino acid motif GGDEF.

Regulon

A set of genes that is controlled by a common transcription factor or regulatory RNA. A regulon usually includes genes that are implicated in a common cellular subsystem or pathway.

AMT-tag proteome database

An accurate mass and time (AMT)-tag proteome database that contains identifications for tryptic peptides based on analysis by capillary liquid chromatography followed by tandem mass spectrometry of various cellular lysates of a single organism.

Core genome

In the context of this Review, the core genome refers to the set of proteins that have been found in each Shewanella genome analysed to date and are of high sequence similarity and are therefore predicted to encode the same function.

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Fredrickson, J., Romine, M., Beliaev, A. et al. Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6, 592–603 (2008). https://doi.org/10.1038/nrmicro1947

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