Regulation of nitrite resistance of the cytochrome cbb3 oxidase by cytochrome c ScyA in Shewanella oneidensis

Yin, Jianhua; Jin, Miao; Zhang, Haiyan; Ju, Lin; Zhang, Lili; Gao, Haichun

doi:10.1002/mbo3.224

Cited by 27 publications

(48 citation statements)

References 66 publications

(239 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We have previously demonstrated that an electron shortage for the cbb 3 oxidase leads to a hyperactive phenotype, as illustrated in a strain deficient of the cytochrome bc 1 complex (Fig. 4B), which functions as a quinol dehydrogenase, mediating electron transfer from the quinol pool to the cbb 3 oxidase1428. Because the cbb 3 oxidase works with electrons either from the cytochrome bc 1 complex or from the Nadi reagents, when electrons are no longer delivered to the cbb 3 oxidase in the absence of the cytochrome bc 1 complex the enzyme exclusively reacts with the Nadi reagents, exhibiting enhanced activity.…”

Section: Resultsmentioning

confidence: 92%

“…As multiple factors are involved in cAMP homeostasis3133, we reasoned that at least some in their altered abundance or absence may suppress nitrite inhibition. In attempts to identify such factors, a random mutation library was constructed from the wild-type strain using pHGT01, a mariner-based transposon vector derived from pFAC2846. This vector has been not only used for construction of transposon insertion libraries but also applicable for cryptic operon screening because of a robust promoter embedded in the transposable sequence2847.…”

Section: Resultsmentioning

confidence: 99%

“…A random mutation library for the S. oneidensis wild-type was constructed with pHGT01, which is a transposon vector with a strong promoter embedded in the transposable region28. Nitrite resistance suppressor strains were selected with gentamycin and 2 mM nitrite.…”

Section: Methodsmentioning

confidence: 99%

“…During aerobic growth of S. oneidensis , the primary target of nitrite is the cytochrome cbb 3 oxidase, the enzyme complex predominantly responsible for oxygen respiration25262728. When non-oxygen EAs are used to support growth, nitrite inhibits respiration of CymA-dependent but not -independent EAs24.…”

mentioning

confidence: 99%

See 3 more Smart Citations

NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool

Jin

Zhang

Sun

et al. 2016

Sci Rep

Self Cite

View full text Add to dashboard Cite

Shewanella, a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by which multiple EAs and their interaction define ecophysiology of these bacteria. Previously, we showed that nitrite inhibits growth of the genus representative Shewanella oneidensis on fumarate and presumably some other CymA (quinol dehydrogenase)-dependent EAs by reducing cAMP production, which in turn leads to lowered expression of nitrite and fumarate reductases. In this study, we demonstrated that inhibition of fumarate growth by nitrite is also attributable to overproduction of NapB, the cytochrome c subunit of nitrate reductase. Further investigations revealed that excessive NapB per se inhibits growth on all EAs tested, including oxygen. When overproduced, NapB acts as an electron shuttle to dissipate electrons of the quinol pool, likely to extracellullar EAs, because the Mtr system, the major electron transport pathway for extracellular electron transport, is implicated. The study not only sheds light on mechanisms by which certain EAs, especially toxic ones, impact the bacterial ecophysiology, but also provides new insights into how electron shuttle c-type cytochromes regulate multi-branched respiratory networks.

show abstract

Section: Resultsmentioning

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool

Jin

Zhang

Sun

et al. 2016

Sci Rep

Self Cite

View full text Add to dashboard Cite

show abstract

“…SOD and peroxidase (POD) activities were measured on the basis of pyrogallol autoxidation and guaiacol as the electron donor, respectively (29,30). Quantitative analysis of cytochrome c oxidase (Cco) was carried out as described previously (31).…”

Section: Methodsmentioning

confidence: 99%

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

Wan

et al. 2015

J Bacteriol

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Physiological Roles of Nitrite and Nitric Oxide in Bacteria: Similar Consequences from Distinct Cell Targets, Protection, and Sensing Systems

Guo

Gao

2021

Advanced Biology

Self Cite

View full text Add to dashboard Cite

sodium nitrite) is currently in a phase 2b clinical trial as a drug for pulmonary hypertension treatment on the basis of the finding that it could be safely applied to reach millimolar concentrations in the airway surface liquid. [6] In the broad nitrogen biogeochemical cycle, nitrite serves as the central molecule linking nitrate (NO 3 − ) to dinitrogen gas (N 2 ) or ammonia (NH 3 ). [7] As a nitrogen oxo-anion, nitrite per se is crucial to life on earth because it participates in diverse key biological processes, especially in bacteria because they are renowned for their ability to carry out biological transformation of nitrite (Maia and Moura, 2014). Nitrite can be oxidized to nitrate or reduced to various nitrogen species such as nitric oxide (NO), nitrous oxide (N 2 O), N 2 , and NH 3 . [8] Although nitrite transformation is regarded as an effective means for detoxification, it brings out new threats. [7] Apart from an intermediate in the nitrogen cycle, NO, whose physiological concentrations are suggested to be up to ≈5 nM in cells, is a well-recognized bacteriostatic agent the same as nitrite. [9] It should be noted that concentrations of NO generated from nitrite reduction vary drastically in different bacteria, for example, less than 20 nM and up to 38 µM in cultures of two denitrifiers Paracoccus denitrificans and Agrobacterium tumefaciens, respectively. [10] In bacteria, a variety of enzymes are implicated in generation of NO from nitrite, and consistently, multiple enzymes contribute to transformation of NO to other nitrogen species for detoxification. [7,11] It is worth noting that in contrast to nitrite, whose transformation is exclusively conducted by enzymes involved in the nitrogen biogeochemical cycle, NO can be generated and scavenged by proteins outside the cycle, bacterial NO synthases (bNOSs) and flavohemoglobin Hmp, respectively. [12] Both nitrite and NO are bacteriostatic agents due to their ability to inhibit protein activity. In vitro studies show that nitrite and NO display similar, albeit not identical, biochemical properties, and therefore proteins susceptible to them are similar, mainly those containing redox-active centers such as heme, iron-sulfur clusters, mono-/di-nuclear iron, thiol, and so on. [13] Consistently, most of cellular targets identified in vivo are metabolic and respiratory enzymes depending on their redox-active centers for catalysis and/or oxi-reduction. [11] Despite this, cellular targets of nitrite and NO in any given bacterial species are Nitrite and nitric oxide (NO) are two active nitrogen oxides that display similar biochemical properties, especially when interacting with redox-sensitive proteins (i.e., hemoproteins), an observation serving as the foundation of the notion that the antibacterial effect of nitrite is largely attributed to NO formation. However, a growing body of evidence suggests that they are largely treated as distinct molecules by bacterial cells. Although both nitrite and NO are formed and decomposed by enzymes participating in the trans...

show abstract

Regulation of nitrite resistance of the cytochrome cbb₃ oxidase by cytochrome c ScyA in Shewanella oneidensis

Cited by 27 publications

References 66 publications

NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool

NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool

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

Physiological Roles of Nitrite and Nitric Oxide in Bacteria: Similar Consequences from Distinct Cell Targets, Protection, and Sensing Systems

Contact Info

Product

Resources

About