Impacts of <i>Shewanella oneidensis c</i>‐type cytochromes on aerobic and anaerobic respiration

Gao, Haichun; Barua, Soumitra; Liang, Yili; Wu, Lian‐Ming; Dong, Yangyang; Reed, Samantha B.; Chen, Jingrong; Culley, David E.; Kennedy, David W.; Yang, Yunfeng; He, Zhili; Nealson, Kenneth H.; Fredrickson, Jim K.; Tiedje, James M.; Romine, Margaret F.; Zhou, Jizhong

doi:10.1111/j.1751-7915.2010.00181.x

Cited by 87 publications

(105 citation statements)

References 45 publications

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“…For the latter, its strategies appear surprisingly clever. The total intracellular iron concentration in S. oneidensis is slightly higher than that in E. coli (ϳ1.8-fold), reflecting a large number of iron-and heme-containing proteins, especially c-type cytochromes (22,68). However, E. coli accumulated 20 times more iron than S. oneidensis in a period of 24 h, suggesting that the latter limits its iron uptake rate (68,72).…”

Section: Discussionmentioning

confidence: 93%

“…S. oneidensis is one of the most radiation-sensitive organisms known, approximately 1 order of magnitude more susceptible to all wavelengths of solar UV, UV, and ionizing radiation than E. coli, a process linked to ROS generation (19)(20)(21). This microorganism possesses a large number of iron-and heme-containing proteins (22,23); it has been proposed that these proteins may be particularly vulnerable upon radiation (24). First, damaged proteins per se may be dysfunctional, directly reducing the ability to survive.…”

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confidence: 99%

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Protection from Oxidative Stress Relies Mainly on Derepression of OxyR-Dependent KatB and Dps in Shewanella oneidensis

Jiang¹,

Dong²,

Luo³

et al. 2013

Journal of Bacteriology

172

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Shewanella thrives in redox-stratified environments where accumulation of H 2 O 2 becomes inevitable because of the chemical oxidation of reduced metals, sulfur species, or organic molecules. As a research model, the representative species Shewanella oneidensis has been extensively studied for its response to various stresses. However, little progress has been made toward an understanding of the physiological and genetic responses of this bacterium to oxidative stress, which is critically relevant to its application as a dissimilatory metal-reducing bacterium. In this study, we systematically investigated the mechanism underlying the response to H 2 O 2 at cellular, genomic, and molecular levels. Using transcriptional profiling, we found that S. oneidensis is hypersensitive to H 2 O 2 in comparison with Escherichia coli, and well-conserved defense genes such as ahpCF, katB, katG, and dps appear to form the first line of defense, whereas iron-sulfur-protecting proteins may not play a significant role. Subsequent identification and characterization of an analogue of the E. coli oxyR gene revealed that S. oneidensis OxyR is the master regulator that mediates the bacterial response to H 2 O 2 -induced oxidative stress by directly repressing or activating the defense genes. The sensitivity of S. oneidensis to H 2 O 2 is likely attributable to the lack of an inducible manganese import mechanism during stress. To cope with stress, major strategies that S. oneidensis adopts include rapid removal of the oxidant and restriction of intracellular iron concentrations, both of which are achieved predominantly by derepression of the katB and dps genes.

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Section: Discussionmentioning

confidence: 93%

mentioning

confidence: 99%

Protection from Oxidative Stress Relies Mainly on Derepression of OxyR-Dependent KatB and Dps in Shewanella oneidensis

Jiang¹,

Dong²,

Luo³

et al. 2013

Journal of Bacteriology

172

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“…For the former, the strategy is to produce multiple scavenging enzymes, with KatB dominating. For the latter, the situation is rather complicated, however, because there are a large number of iron-and heme-containing proteins in S. oneidensis (such as up to 42 c-type cytochromes, while E. coli has 5 to 7), thus requiring relatively high levels of iron for its normal physiological activities (54,55).…”

Section: Discussionmentioning

confidence: 99%

A Matter of Timing: Contrasting Effects of Hydrogen Sulfide on Oxidative Stress Response in Shewanella oneidensis

Wan

et al. 2015

J Bacteriol

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Hydrogen sulfide (H 2 S), well known for its toxic properties, has recently become a research focus in bacteria, in part because it has been found to prevent oxidative stress caused by treatment with some antibiotics. H 2 S has the ability to scavenge reactive oxygen species (ROS), thus preventing oxidative stress, but it is also toxic, leading to conflicting reports of its effects in different organisms. Here, with Shewanella oneidensis as a model, we report that the effects of H 2 S on the response to oxidative stress are time dependent. When added simultaneously with H 2 O 2 , H 2 S promoted H 2 O 2 toxicity by inactivating catalase, KatB, a hemecontaining enzyme involved in H 2 O 2 degradation. Such an inhibitory effect may apply to other heme-containing proteins, such as cytochrome cbb 3 oxidase. When H 2 O 2 was supplied 20 min or later after the addition of H 2 S, the oxidative-stress-responding regulator OxyR was activated, resulting in increased resistance to H 2 O 2 . The activation of OxyR was likely triggered by the influx of iron, a response to lowered intracellular iron due to the iron-sequestering property of H 2 S. Given that Shewanella bacteria thrive in redox-stratified environments that have abundant sulfur and iron species, our results imply that H 2 S is more important for bacterial survival in such environmental niches than previously believed. IMPORTANCE Previous studies have demonstrated that H 2 S is either detrimental or beneficial to bacterial cells. While it can act as a growth-inhibiting molecule by damaging DNA and denaturing proteins, it helps cells to combat oxidative stress. Here we report that H 2 S indeed has these contrasting biological functions and that its effects are time dependent. Immediately after H 2 S treatment, there is growth inhibition due to damage of heme-containing proteins, at least to catalase and cytochrome c oxidase. In contrast, when added a certain time later, H 2 S confers an enhanced ability to combat oxidative stress by activating the H 2 O 2 -responding regulator OxyR. Our data reconcile conflicting observations about the functions of H 2 S.

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“…S. oneidensis MR-1 is a facultative anaerobic, non- ϩϩ (8) ϩϩ (8) Ϫ (8) ϩϩϩ (8) ✓ (10) Fe(III) oxide ϩϩϩ (37) ϩϩϩ (37) ϩϩ (37) ϩϩ (52) ϩϩ ( (34) ϩϩ (13) ϩ (13) Ϫ (13) ϩϩϩ (13) / (10) Mn(IV) oxide ϩϩϩ (53) ϩϩ (53) ϩϩ (52) ✓ (66) ✓ (34) ϩϩ (4,8,22) ϩϩ (8,22) ϩϩ (8,22) ϩϩ (8,22) Ferric citrate ϩϩϩ (37)…”

Section: Extracellular Electron Acceptorsmentioning

confidence: 99%

Dissimilatory Reduction of Extracellular Electron Acceptors in Anaerobic Respiration

Richter

Schicklberger

Gescher

2012

Appl Environ Microbiol

246

181

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An extension of the respiratory chain to the cell surface is necessary to reduce extracellular electron acceptors like ferric iron or manganese oxides. In the past few years, more and more compounds were revealed to be reduced at the surface of the outer membrane of Gram-negative bacteria, and the list does not seem to have an end so far. Shewanella as well as Geobacter strains are model organisms to discover the biochemistry that enables the dissimilatory reduction of extracellular electron acceptors. In both cases, c-type cytochromes are essential electron-transferring proteins. They make the journey of respiratory electrons from the cytoplasmic membrane through periplasm and over the outer membrane possible. Outer membrane cytochromes have the ability to catalyze the last step of the respiratory chains. Still, recent discoveries provided evidence that they are accompanied by further factors that allow or at least facilitate extracellular reduction. This review gives a condensed overview of our current knowledge of extracellular respiration, highlights recent discoveries, and discusses critically the influence of different strategies for terminal electron transfer reactions.

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Impacts of Shewanella oneidensis c‐type cytochromes on aerobic and anaerobic respiration

Cited by 87 publications

References 45 publications

Protection from Oxidative Stress Relies Mainly on Derepression of OxyR-Dependent KatB and Dps in Shewanella oneidensis

Protection from Oxidative Stress Relies Mainly on Derepression of OxyR-Dependent KatB and Dps in Shewanella oneidensis

A Matter of Timing: Contrasting Effects of Hydrogen Sulfide on Oxidative Stress Response in Shewanella oneidensis

Dissimilatory Reduction of Extracellular Electron Acceptors in Anaerobic Respiration

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