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

Jin, Miao; Zhang, Qianyun; Sun, Yijuan; Gao, Haichun

doi:10.1038/srep37456

Cited by 17 publications

(13 citation statements)

References 66 publications

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“…By this logic, we focus on the respiratory chain, especially terminal oxidases. This coincides with the findings of systematic investigations into nitrite and NO physiology in Shewanella oneidensis, a facultative Gram-negative γ-proteobacterium renowned for respiratory versatility [15][16][17][18][19][20] . In this bacterium, the primary target of nitrite is heme-copper oxidase (HCO) cbb 3 (hereafter referred to as cbb 3 ), whereas NO indistinguishably interacts with all cytochromes c 15,16,19,20 .…”

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confidence: 86%

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Nitrite modulates aminoglycoside tolerance by inhibiting cytochrome heme-copper oxidase in bacteria

et al. 2020

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As a bacteriostatic agent, nitrite has been used in food preservation for centuries. When used in combination with antibiotics, nitrite is reported to work either cooperatively or antagonistically. However, the mechanism underlying these effects remains largely unknown. Here we show that nitrite mediates tolerance to aminoglycosides in both Gram-negative and Gram-positive bacteria, but has little interaction with other types of antibiotics. Nitrite directly and mainly inhibits cytochrome heme-copper oxidases (HCOs), and by doing so, the membrane potential is compromised, blocking uptake of aminoglycosides. In contrast, reduced respiration (oxygen consumption rate) resulting from nitrite inhibition is not critical for aminoglycoside tolerance. While our data indicate that nitrite is a promising antimicrobial agent targeting HCOs, cautions should be taken when used with other antibiotics, aminoglycosides in particular.

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confidence: 86%

“…These data, all together, manifest that nitrite modulates aminoglycoside susceptibility by compromising cbb 3based respiration, implying that cbb 3 , the bc 1 complex, or both could be targets of nitrite. This study focused on cbb 3 , because it has been shown to be susceptible to nitrite [15][16][17][18][19][20] .…”

Section: Resultsmentioning

confidence: 99%

Nitrite modulates aminoglycoside tolerance by inhibiting cytochrome heme-copper oxidase in bacteria

et al. 2020

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“…Distinct susceptibilities of S. oneidensis and E. coli to nitrite and NO. Previously, we demonstrated that S. oneidensis is highly susceptible to nitrite (NaNO 2 and KNO 2 ) during aerobiosis (29)(30)(31)(32). For comparison, we assessed the susceptibility of E. coli to nitrite under the same conditions ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Consistently, nitrite has been found to be extremely toxic to S. oneidensis cells grown under either aerobic or anaerobic conditions. While the primary target of nitrite for oxygen respiration is heme-copper oxidase (HCO) cyt cbb 3 , nitrite inhibition of alternative EA respiration involves cAMP-Crp (catabolite repression protein) regulation and NapB, a soluble c-type cyt that, in excess, dissipates electrons of the quinol pool (29)(30)(31).…”

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Distinct Nitrite and Nitric Oxide Physiologies in Escherichia coli and Shewanella oneidensis

Quanfei

Yin

Jin

et al. 2018

Appl Environ Microbiol

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Nitrite has been used as a bacteriostatic agent for centuries in food preservation. It is widely accepted that this biologically inert molecule functions indirectly, serving as a stable reservoir of bioactive nitric oxide (NO) and other reactive nitrogen species to impact physiology. As a result, to date, we know surprisingly little about targets of nitrite. Here, we carry out comparative analyses of nitrite and NO physiology in and in , a Gram-negative environmental bacterium renowned for respiratory versatility. These two bacteria differ from each other in many aspects of nitrite and NO physiology, including NO generation, NO degradation, and unexpectedly, their contrary susceptibility to nitrite and NO. In cell extracts of both bacteria, most of the NO targets are also susceptible to nitrite, and vice versa. However, with respect to growth inhibition caused by NO, the targets are impacted distinctly; NO targets are responsible for the inhibition of growth of but not of More surprisingly, all proteins identified to be implicated in NO tolerance in other bacteria appear to play a dispensable role in protecting against NO. These data suggest that is equipped with a robust but yet unknown NO protecting system. In the case of nitrite, it is clear that the target of physiological significance in both bacteria is cytochrome heme-copper oxidase. Nitrite is toxic to living organisms at high levels, but such antibacterial effects of nitrite are attributable to the formation of nitric oxide (NO), a highly reactive radical gas molecule. Here, we report that is highly resistant to NO but sensitive to nitrite compared to by approximately 4-fold. In both bacteria, nitrite inhibits bacterial growth by targeting cytochrome heme-copper oxidase. In contrast, the targets of NO are diverse. Although these targets are similar in and, they are responsible for growth inhibition caused by NO in the former but not in the latter. Overall, the presented data, along with the previous data, solidify a proposal that the targets of NO and nitrite in bacteria are largely different.

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“…In S. oneidensis, the primary target of nitrite has been identified as cytochrome cbb 3 , an HCO that is highly efficient for oxygen respiration (22)(23)(24). For respiration of nonoxygen electron acceptors (EAs), nitrite inhibition involves cyclic AMP-catabolite repression protein (cAMP-Crp) regulation and NapB, a soluble cytochrome c that in excess dissipates electrons of the quinol pool (25,26).…”

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Cytochromes c Constitute a Layer of Protection against Nitric Oxide but Not Nitrite

Quanfei

Sun

Gao

2018

Appl Environ Microbiol

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Nitric oxide (NO) is a radical gas that reacts with various biological molecules in complex ways to inhibit growth as a bacteriostatic agent. NO is nearly ubiquitous because it can be generated both biotically and abiotically. To protect the cell from NO damage, bacteria have evolved many strategies, with the production of detoxifying enzymatic systems being the most efficient. Here, we report that -type cytochromes (cytochromes) constitute a primary NO protection system in , a Gram-negative environmental bacterium renowned for respiratory versatility due to its high cytochrome content. By using mutants producing cytochromes at varying levels, we found that the content of these proteins is inversely correlated with the growth inhibition imposed by NO, whereas the effect of each individual cytochrome is negligible. This NO-protecting system has no effect on nitrite inhibition. In the absence of cytochromes , other NO targets and protective proteins, such as NnrS, emerge to show physiological influences during the NO stress. We further demonstrate that cytochromes also play a similar role in , albeit only modestly. Our data thus identify the function of an important group of proteins in alleviating NO stress. It is widely accepted that the antibacterial effects of nitrite are attributable to nitric oxide (NO) formation, suggesting a correlation of bacterial susceptibilities to these two chemicals. However, compared to , is highly sensitive to nitrite but resistant to NO, implying the presence of robust NO-protective systems. Here, we show that -type cytochromes (cytochromes) play a main role in protecting against damages from NO but not from nitrite. In their absence, impacts of proteins that promote NO tolerance and that are targets of NO inhibition become evident. Our data thus reveal the specific activity of cytochromes in alleviating the stress caused by NO but not nitrite.

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

Cited by 17 publications

References 66 publications

Nitrite modulates aminoglycoside tolerance by inhibiting cytochrome heme-copper oxidase in bacteria

Nitrite modulates aminoglycoside tolerance by inhibiting cytochrome heme-copper oxidase in bacteria

Distinct Nitrite and Nitric Oxide Physiologies in Escherichia coli and Shewanella oneidensis

Cytochromes c Constitute a Layer of Protection against Nitric Oxide but Not Nitrite

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