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      Transcriptional mechanisms for differential expression of outer membrane cytochrome genes omcA and mtrC in Shewanella oneidensis MR-1

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          Abstract

          Background

          Shewanella oneidensis MR-1 is capable of reducing extracellular electron acceptors, such as metals and electrodes, through the Mtr respiratory pathway, which consists of the outer membrane cytochromes OmcA and MtrC and associated proteins MtrA and MtrB. These proteins are encoded in the mtr gene cluster ( omcA- mtrCAB) in the MR-1 chromosome.

          Results

          Here, we investigated the transcriptional mechanisms for the mtr genes and demonstrated that omcA and mtrC are transcribed from two upstream promoters, P omcA and P mtrC , respectively. In vivo transcription and in vitro electrophoretic mobility shift assays revealed that a cAMP receptor protein (CRP) positively regulates the expression of the mtr genes by binding to the upstream regions of P omcA and P mtrC . However, the expression of omcA and mtrC was differentially regulated in response to culture conditions; specifically, the expression from P mtrC was higher under aerobic conditions than that under anaerobic conditions with fumarate as an electron acceptor, whereas expression from P omcA exhibited the opposite trend. Deletion of the region upstream of the CRP-binding site of P omcA resulted in a significant increase in promoter activity under aerobic conditions, demonstrating that the deleted region is involved in the negative regulation of P omcA .

          Conclusions

          Taken together, the present results indicate that transcription of the mtr genes is regulated by multiple promoters and regulatory systems, including the CRP/cAMP-dependent regulatory system and yet-unidentified negative regulators.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12866-015-0406-8) contains supplementary material, which is available to authorized users.

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          Most cited references58

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          Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.

          Three kinds of improvements have been introduced into the M13-based cloning systems. (1) New Escherichia coli host strains have been constructed for the E. coli bacteriophage M13 and the high-copy-number pUC-plasmid cloning vectors. Mutations introduced into these strains improve cloning of unmodified DNA and of repetitive sequences. A new suppressorless strain facilitates the cloning of selected recombinants. (2) The complete nucleotide sequences of the M13mp and pUC vectors have been compiled from a number of sources, including the sequencing of selected segments. The M13mp18 sequence is revised to include the G-to-T substitution in its gene II at position 6 125 bp (in M13) or 6967 bp in M13mp18. (3) M13 clones suitable for sequencing have been obtained by a new method of generating unidirectional progressive deletions from the polycloning site using exonucleases HI and VII.
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            Secretion of flavins by Shewanella species and their role in extracellular electron transfer.

            Fe(III)-respiring bacteria such as Shewanella species play an important role in the global cycle of iron, manganese, and trace metals and are useful for many biotechnological applications, including microbial fuel cells and the bioremediation of waters and sediments contaminated with organics, metals, and radionuclides. Several alternative electron transfer pathways have been postulated for the reduction of insoluble extracellular subsurface minerals, such as Fe(III) oxides, by Shewanella species. One such potential mechanism involves the secretion of an electron shuttle. Here we identify for the first time flavin mononucleotide (FMN) and riboflavin as the extracellular electron shuttles produced by a range of Shewanella species. FMN secretion was strongly correlated with growth and exceeded riboflavin secretion, which was not exclusively growth associated but was maximal in the stationary phase of batch cultures. Flavin adenine dinucleotide was the predominant intracellular flavin but was not released by live cells. The flavin yields were similar under both aerobic and anaerobic conditions, with total flavin concentrations of 2.9 and 2.1 micromol per gram of cellular protein, respectively, after 24 h and were similar under dissimilatory Fe(III)-reducing conditions and when fumarate was supplied as the sole electron acceptor. The flavins were shown to act as electron shuttles and to promote anoxic growth coupled to the accelerated reduction of poorly crystalline Fe(III) oxides. The implications of flavin secretion by Shewanella cells living at redox boundaries, where these mineral phases can be significant electron acceptors for growth, are discussed.
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              Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation.

              Dissimilatory iron and/or manganese reduction is known to occur in several organisms, including anaerobic sulfur-reducing organisms such as Geobacter metallireducens or Desulfuromonas acetoxidans, and facultative aerobes such as Shewanella putrefaciens. These bacteria couple both carbon oxidation and growth to the reduction of these metals, and inhibitor and competition experiments suggest that Mn(IV) and Fe(III) are efficient electron acceptors similar to nitrate in redox abilities and capable of out-competing electron acceptors of lower potential, such as sulfate (sulfate reduction) or CO2 (methanogenesis). Field studies of iron and/or manganese reduction suggest that organisms with such metabolic abilities play important roles in coupling the oxidation of organic carbon to metal reduction under anaerobic conditions. Because both iron and manganese oxides are solids or colloids, they tend to settle downward in aquatic environments, providing a physical mechanism for the movement of oxidizing potential into anoxic zones. The resulting biogeochemical metal cycles have a strong impact on many other elements including carbon, sulfur, phosphorous, and trace metals.
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                Author and article information

                Contributors
                s096051@toyaku.ac.jp
                akouzuma@toyaku.ac.jp
                anojiri@mail.ecc.u-tokyo.ac.jp
                kazuyaw@toyaku.ac.jp
                Journal
                BMC Microbiol
                BMC Microbiol
                BMC Microbiology
                BioMed Central (London )
                1471-2180
                21 March 2015
                21 March 2015
                2015
                : 15
                : 68
                Affiliations
                [ ]School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, 192-0392 Tokyo Japan
                [ ]Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, 113-8657 Tokyo Japan
                Article
                406
                10.1186/s12866-015-0406-8
                4417206
                25886963
                1f520f3c-7675-46f6-9a4d-7e803cc63257
                © Kasai et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 27 November 2014
                : 11 March 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Microbiology & Virology
                extracellular electron transfer,outer membrane cytochrome,transcriptional regulation,shewanella

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