Periplasmic Electron Transfer via the
            <i>c</i>
            -Type Cytochromes MtrA and FccA of
            <i>Shewanella oneidensis</i>
            MR-1

Schuetz, Bjoern; Schicklberger, Marcus; Kuermann, Johannes; Spormann, Alfred M.; Gescher, Johannes

doi:10.1128/aem.01834-09

Cited by 149 publications

(138 citation statements)

References 29 publications

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“…The fccA (SO0970) gene in S. oneidensis has been shown to be a major soluble fumarate reductase during anaerobic growth (39), but fccA expression was not significantly up-expressed at the transcriptional level in wild-type or mutant cultures under the tested conditions. However, recent work has shown that FccA might be involved in multiple periplasmic electron transfer networks (48). It should be noted that gene expression was done with cultures that had been grown aerobically and then transferred to anoxic conditions; therefore, gene expression for some genes may differ from those reported in previous studies that have used cultures grown in prereduced, anaerobic medium for longer time periods.…”

Section: Resultscontrasting

confidence: 40%

Shewanella oneidensis MR-1 Sensory Box Protein Involved in Aerobic and Anoxic Growth

Sundararajan

Kurowski

Yan

et al. 2011

Appl Environ Microbiol

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Although little is known of potential function for conserved signaling proteins, it is hypothesized that such proteins play important roles to coordinate cellular responses to environmental stimuli. In order to elucidate the function of a putative sensory box protein (PAS domains) in Shewanella oneidensis MR-1, the physiological role of SO3389 was characterized. The predicted open reading frame (ORF) encodes a putative sensory box protein that has PAS, GGDEF, and EAL domains, and an in-frame deletion mutant was constructed (⌬SO3389) with approximately 95% of the ORF deleted. Under aerated conditions, wild-type and mutant cultures had similar growth rates, but the mutant culture had a lower growth rate under static, aerobic conditions. Oxygen consumption rates were lower for mutant cultures (1.5-fold), and wild-type cultures also maintained lower dissolved oxygen concentrations under aerated growth conditions. When transferred to anoxic conditions, the mutant did not grow with fumarate, iron(III), or dimethyl sulfoxide (DMSO) as electron acceptors. Biochemical assays demonstrated the expression of different c-type cytochromes as well as decreased fumarate reductase activity in the mutant transferred to anoxic growth conditions. Transcriptomic studies showed the inability of the mutant to up-express and down-express genes, including c-type cytochromes (e.g., SO4047/SO4048, SO3285/SO3286), reductases (e.g., SO0768, SO1427), and potential regulators (e.g., SO1329). The complemented strain was able to grow when transferred from aerobic to anoxic growth conditions with the tested electron acceptors. The modeled structure for the SO3389 PAS domains was highly similar to the crystal structures of FAD-binding PAS domains that are known O 2 /redox sensors. Based on physiological, genomic, and bioinformatic results, we suggest that the sensory box protein, SO3389, is an O 2 /redox sensor that is involved in optimization of aerobic growth and transitions to anoxia in S. oneidensis MR-1.In the postgenomic era, uncharacterized genes pose a major challenge in biology (16), and many sequenced genomes still contain a large fraction (up to 30 to 40%) of genes without defined physiological roles (13). In fact, many aspects of signaling and stress response most likely reside in this fraction of genes for a given organism and underlie the lack of understanding in physiological responses and control of metabolism. Many uncharacterized genes/proteins are classified as sensory box proteins based upon conserved domains, but signals and cellular responses for most presumptive sensory box proteins are not known.Shewanella oneidensis MR-1, a facultative anaerobe classified as a gammaproteobacterium, can utilize numerous inorganic compounds as electron acceptors (e.g., oxygen, nitrate, and metals). The S. oneidensis MR-1 genome sequence was determined (20), and the most recent annotation of the 5.1-Mb genome estimated 4,467 genes, of which 1,623 had hypothetical functions (28). Many bacteria considered to be "environmental" organisms typica...

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Section: Resultscontrasting

confidence: 40%

Shewanella oneidensis MR-1 Sensory Box Protein Involved in Aerobic and Anoxic Growth

Sundararajan

Kurowski

Yan

et al. 2011

Appl Environ Microbiol

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“…Interestingly, the fumarate reductase FccA and the small tetraheme cytochrome (STC) (CctA) are highly abundant in the periplasm under anoxic conditions (Tsapin et al, 2001;Meyer et al, 2004). Nevertheless, although it was suggested that they might have a role in the transfer of electrons to the outer membrane, a corresponding phenotype under conditions of ferric iron or dimethyl sulfoxide (DMSO) reduction was not shown so far (Gordon et al, 2000;Schuetz et al, 2009;Fonseca et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…The preparation of periplasmic and membrane fractions was performed as described by Schuetz et al (2009). The expression of the c-type cytochromes was monitored via SDS-PAGE coupled with a heme-linked peroxidase stain as previously described (Thomas et al, 1976).…”

Section: Cell Fractionationmentioning

confidence: 99%

“…Unsurprisingly, a cymA-deficient mutant shows growth deficiencies with a variety of anoxic electron acceptors (Myers and Myers, 1997). Although it was shown experimentally in vivo and in vitro that CymA can directly transfer electrons to the respiratory fumarate reductase FccA, it was suggested that a direct transfer would also be in place toward the periplasmic nitrate and nitrite reductases NapAB and NrfA, respectively (Schwalb et al, 2002;Gao et al, 2009;Schuetz et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime

et al. 2015

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Microorganisms show an astonishing versatility in energy metabolism. They can use a variety of different catabolic electron acceptors, but they use them according to a thermodynamic hierarchy, which is determined by the redox potential of the available electron acceptors. This hierarchy is reflected by a regulatory machinery that leads to the production of respiratory chains in dependence of the availability of the corresponding electron acceptors. In this study, we showed that the c-proteobacterium Shewanella oneidensis produces several functional electron transfer chains simultaneously. Furthermore, these chains are interconnected, most likely with the aid of c-type cytochromes. The cytochrome pool of a single S. oneidensis cell consists of ca. 700 000 hemes, which are reduced in the absence on an electron acceptor, but can be reoxidized in the presence of a variety of electron acceptors, irrespective of prior growth conditions. The small tetraheme cytochrome (STC) and the soluble heme and flavin containing fumarate reductase FccA have overlapping activity and appear to be important for this electron transfer network. Double deletion mutants showed either delayed growth or no growth with ferric iron, nitrate, dimethyl sulfoxide or fumarate as electron acceptor. We propose that an electron transfer machinery that is produced irrespective of a thermodynamic hierarchy not only enables the organism to quickly release catabolic electrons to a variety of environmental electron acceptors, but also offers a fitness benefit in redox-stratified environments.

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“…Menaquinol is in turn oxidized by the inner membrane‐bound quinol dehydrogenase CymA (Marritt et al ., 2012), or in its absence, the enzyme complex SirCD (Cordova et al ., 2011). Next, electrons are transferred across the periplasmic space by diffusible c ‐cytochromes STC and FccA (Schuetz et al ., 2009; Fonseca et al ., 2013) and transferred to terminal reductases at the outer membrane such as MtrA and MtrC which are associated with the MtrCAB complex (Fig. 1) (Coursolle and Gralnick, 2010; Breuer et al ., 2015).…”

Section: Introductionmentioning

confidence: 99%

Towards patterned bioelectronics: facilitated immobilization of exoelectrogenic Escherichia coli with heterologous pili

Lienemann

TerAvest

Pitkänen

et al. 2018

Microbial Biotechnology

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SummaryBiosensors detect signals using biological sensing components such as redox enzymes and biological cells. Although cellular versatility can be beneficial for different applications, limited stability and efficiency in signal transduction at electrode surfaces represent a challenge. Recent studies have shown that the Mtr electron conduit from Shewanella oneidensis MR‐1 can be produced in Escherichia coli to generate an exoelectrogenic model system with well‐characterized genetic tools. However, means to specifically immobilize this organism at solid substrates as electroactive biofilms have not been tested previously. Here, we show that mannose‐binding Fim pili can be produced in exoelectrogenic E. coli and can be used to selectively attach cells to a mannose‐coated material. Importantly, cells expressing fim genes retained current production by the heterologous Mtr electron conduit. Our results demonstrate the versatility of the exoelectrogenic E. coli system and motivate future work that aims to produce patterned biofilms for bioelectronic devices that can respond to various biochemical signals.

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Periplasmic Electron Transfer via the c -Type Cytochromes MtrA and FccA of Shewanella oneidensis MR-1

Cited by 149 publications

References 29 publications

Shewanella oneidensis MR-1 Sensory Box Protein Involved in Aerobic and Anoxic Growth

Shewanella oneidensis MR-1 Sensory Box Protein Involved in Aerobic and Anoxic Growth

A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime

Towards patterned bioelectronics: facilitated immobilization of exoelectrogenic Escherichia coli with heterologous pili

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