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Towards Environmental Systems Biology of Shewanella

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Towards Environmental Systems Biology of Shewanella REVIEWS SYSTEMS MICROBIOLOGY Towards environmental systems biology of Shewanella James K. Fredrickson*, Margaret F. Romine*, Alexander S. Beliaev*, Jennifer M. Auchtung‡, Michael E. Driscoll§, Timothy S. Gardner§, Kenneth H. Nealson||, Andrei L. Osterman¶, Grigoriy Pinchuk*, Jennifer L. Reed#, Dmitry A. Rodionov¶, Jorge L. M. Rodrigues**, Daad A. Saffarini‡‡, Margrethe H. Serres§§, Alfred M. Spormann||||, Igor B. Zhulin¶¶ and James M. Tiedje‡ 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. 17 18 Dissimilatory The modern-day Shewanella era began in 1988 with the tellurite and vanadate , and even the reduction of 19,20 An enzymatic reaction in which publication of the description of Shewanella oneidensis nitroaromatic compounds by some strains . These a compound is oxidized or MR-1 (formerly Alteromonas putrefaciens), which diverse metabolic capabilities provide shewanellae with reduced but is not assimilated was capable of dissimilatory metabolism of manganese considerable potential for the remediation of environ- or incorporated into cells for 1 21 the purposes of biosynthesis and iron oxides . Among the notable properties of ments that are contaminated with radionuclides . during, for example, S. oneidensis MR-1 was its ability to transfer electrons to Furthermore, our analyses of the genome sequences of respiration. solid metal oxides and its remarkable anaerobic versatil- various strains suggest that, collectively, the shewanellae ity (it can use more than ten different electron acceptors). can use a broad range of carbon substrates. Given their Electron acceptor It also produced sulphide from thiosulphate (an almost widespread distribution in environments where organic An oxidant used during cellular respiration. diagnostic trait for the Shewanella group) and reduced matter is actively degraded, shewanellae should also prove elemental sulphur, a property that is not commonly useful as model organisms for obtaining systems-level associated with facultative aerobic bacteria. Isolation insights into carbon-cycling processes. of similar microorganisms soon followed: abundant Shewanellae are common members of complex com- populations were identified at redox interfaces in the munities in aquatic and sedimentary systems that are Black Sea2 and many other marine3,4 and non-marine5–7 chemically stratified on a permanent or seasonal basis22. *Biological Sciences Division, shewanellae were found to be iron and manganese reduc- To be competitive in such environments and to respond Pacific Northwest National ers. In fact, shewanellae had been in culture collections to the available resources, shewanellae must have robust Laboratory, Richland, since the middle of the twentieth century, but were iden- sensing and regulatory systems. Therefore, genome-centric Washington 99352, USA. tified as Pseudomonas (or Alteromonas) putrefaciens5–8. approaches are being used to study these systems in order ‡Center for Microbial Ecology, Michigan State What was new was the discovery of its reductive capaci- of increasing complexity, from individual genes and University, East Lansing, ties, although there were many clues to its dissimilatory operons to populations and communities. Because most Michigan 48824, USA. abilities in several publications before its recognition as studies have used genetics and genomics to understand Correspondence to J.K.F. Shewanella in the late 1980s6,8–11. metabolism and regulation, initial systems analyses have and J.M.T. It was soon realized that the versatility of Shewanella spp. focused on S. oneidensis MR-1, the first genome of the e-mails: jim.fredrickson@ 23 pnl.gov; [email protected] extended to other ‘non-standard’ metal electron acceptors, shewanellae to be sequenced . These analyses have used 3 12 13 doi:10.1038/nrmicro1947 such as uranium [U(VI)] , chromium [Cr(VI)] , iodate , complementary top-down and bottom-up approaches. Published online 7 July 2008 technetium14, neptunium15, plutonium16, selenite17, In top-down investigations, bioinformatics-based 592 | august 2008 | VOLumE 6 www.nature.com/reviews/micro © 2008 Macmillan Publishers Limited. All rights reserved. FOCUS ON SUSTAINABREVIEWSILITY Author addresses if available, not all of the predictions and conjectures reported here have been tested experimentally. §Program in Bioinformatics, Boston University, Boston, Massachusetts 02215, USA. || Department of Earth Sciences, University of Southern California, Los Angeles, Developing systems-level understanding California 90089, USA. Sensing, signal transduction and regulation. Signal- ¶Burnham Institute for Medical Research, La Jolla, California 92037, USA. #Department of Chemical and Biological Engineering, University of Wisconsin, Madison, transduction regulatory systems link extracellular and Wisconsin 53706, USA. intracellular cues to cellular responses through networks **Department of Biology, University of Texas, Arlington, Texas 76019, USA. that consist of receptors, transmitters of information and ‡‡Department of Biological Sciences, University of Wisconsin, Milwaukee, Wisconsin regulators. Because of the ability of Shewanella species to 53211, USA. thrive in a range of carbon-resource and redox environ- §§Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine ments, metabolic and regulatory plasticity seems to be Biological Laboratory, Woods Hole, Massachusetts 02543, USA. one of the keys to the ecological success of the species. |||| Departments of Biological Sciences, Chemical Engineering, Civil and Environmental Indeed, analysis of the S. oneidensis strain MR-1 genome Engineering, and Geological and Environmental Sciences, Stanford University, Stanford, sequence23 identified 211 one-component systems and 47 California 94305, USA. two-component systems, which supports the proposed com- ¶¶Joint Institute for Computational Sciences, The University of Tennessee — Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA. plexity of the energy-conversion pathways in this organ- ism. Most of our information on sensing and regulation in Shewanella spp. has come from computational predic- genome functional predictions are made using a range tions, which, in turn, provide targets for experimental val- of tools and resources (TABLE 1); high-throughput idation and further understanding of signal-transduction expression analyses and functional genomics also uncover complexity. One tool that is useful for the study of these key genes, as well as metabolic and regulatory networks. systems is the microbial signal-transduction (MiST) The bottom-up component uses genetic, physiological database24 (TABLE 1), which contains detailed informa- and biochemical approaches to test or verify predictions tion on predicted signal-transduction genes and proteins made by the top-down approaches. The coupling of top- from hundreds of microbial genomes and has allowed down and bottom-up approaches provides a powerful S. oneidensis MR-1 to be compared with Escherichia coli way to describe the function and regulation of metabolic and other model organisms. subsystems and, ultimately, to link these subsystems to descriptions of signal-transduction and transcriptional One- and two-component systems. Protein-sequence regulatory systems. analyses combined with cross-genome and inter- Although research efforts have largely focused on genome comparisons revealed that three classes of S. oneidensis MR-1, investigations of shewanellae are signal-transduction proteins are significantly enriched being extended to other members of the genus and are in S. oneidensis MR-1 compared with most other One-component system taking advantage of the availability of genome sequences sequenced gammaproteobacteria: chemotaxis pro- A regulatory protein that from 23 other Shewanella strains that are either com- teins, sensors that contain PAS domains (the ubiquitous combines both sensory and (TABLE 2) regulatory capabilities that plete or in progress . This has allowed the use sensory domain that has been implicated in detecting usually reside in two distinct of comparative genomics to gain insight into the evolu- environmental signals, such as light, oxygen and chemi- domains. The repressor of the tion and environmental adaptations of members of the cals that affect the redox potential25) and modulators of lactose operons (LacI) and the genus. The availability of such a large number of related second-messenger cyclic nucleotide signalling. catabolite activator protein of genome sequences provides the basis for improving our In contrast to E. coli, which uses a single set of chemo- Escherichia coli are classical 26 examples. systems-level analysis and understanding of S. oneidensis taxis genes and only five dedicated chemoreceptors , MR-1 and for developing a systems-level understanding S. oneidensis MR-1 is predicted
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