Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: Heme d binds CO with high affinity

Borisov, Vitaliy B.

doi:10.1134/s0006297908010021

Cited by 49 publications

(40 citation statements)

References 79 publications

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“…The presence of the cytochrome bd complex in the ECOM4-AmuCytbd complemented strain was confirmed using a spectrum measurement that showed a major peak at 430 nm, which is in line with the Soret peak of cytochrome bd (Fig. 5B), as previously described (32,33). To determine if the oxygen reduction was heme dependent and thus cytochrome bd dependent, three parallel fermentors containing medium with or without hemin were used.…”

Section: Resultssupporting

confidence: 63%

Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer

Ouwerkerk

Ark

Davids

et al. 2016

Appl Environ Microbiol

119

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Akkermansia muciniphila colonizes the mucus layer of the gastrointestinal tract, where the organism can be exposed to the oxygen that diffuses from epithelial cells. To understand how A. muciniphila is able to survive and grow at this oxic-anoxic interface, its oxygen tolerance and response and reduction capacities were studied. A. muciniphila was found to be oxygen tolerant. On top of this, under aerated conditions, A. muciniphila showed significant oxygen reduction capacities and its growth rate and yield were increased compared to those seen under strict anaerobic conditions. Transcriptome analysis revealed an initial oxygen stress response upon exposure to oxygen. Thereafter, genes related to respiration were expressed, including those coding for the cytochrome bd complex, which can function as a terminal oxidase. The functionality of A. muciniphila cytochrome bd genes was proven by successfully complementing cytochrome-deficient Escherichia coli strain ECOM4. We conclude that A. muciniphila can use oxygen when it is present at nanomolar concentrations. IMPORTANCEThis article explains how Akkermansia muciniphila, previously described as a strictly anaerobic bacterium, is able to tolerate and even benefit from low levels of oxygen. Interestingly, we measured growth enhancement of A. muciniphila and changes in metabolism as a result of the oxygen exposure. In this article, we discuss similarities and differences of this oxygen-responsive mechanism with respect to those of other intestinal anaerobic isolates. Taken together, we think that these are valuable data that indicate how anaerobic intestinal colonizing bacteria can exploit low levels of oxygen present in the mucus layer and that our results have direct relevance for applicability, as addition of low oxygen concentrations could benefit the in vitro growth of certain anaerobic organisms.T he gastrointestinal (GI) tract harbors a rich and diverse microbial community, which has proven to play a role in host health and physiology (1). This microbial community is not in direct contact with epithelial cells; a thin layer of host-derived mucus separates them. The outer layer of mucus is colonized with microbes that differ in composition from the luminal microbiota (2, 3). The mucin glycans are used by some bacteria as growth substrates, resulting in the production of short-chain fatty acids (SCFAs) (4). To the host, the SCFAs are important modulators of gut health (4). To the microbial community, SCFAs are a necessary waste product, and the process of SCFA production is required to maintain the redox balance in the cell, as it can restore the NAD ϩ /NADH ratio (5). One member of the mucosa-associated microbiota is Akkermansia muciniphila, a mucin-degrading specialist that can use mucin as a sole carbon and nitrogen source (6). A. muciniphila is associated with a healthy GI tract, as its abundance is inversely correlated with several GI tract-related disorders (7). Moreover, it has been shown that A. muciniphila has immune-stimulatory capacities, stimul...

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Section: Resultssupporting

confidence: 63%

Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer

Ouwerkerk

Ark

Davids

et al. 2016

Appl Environ Microbiol

119

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“…1, inset). Such peculiar W-shape is consistently observed as well in static Soret difference absorption spectra of CO binding to the enzyme in the R state [38, 40, 52, 55, 56]. …”

Section: Resultsmentioning

confidence: 66%

Heme–heme and heme–ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy

Rappaport

Zhang

Vos

et al. 2010

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Summary Cytochrome bd is a terminal quinol:O2 oxidoreductase of respiratory chains of many bacteria. It contains three hemes, b558, b595, and d. The role of heme b595 remains obscure. A CO photolysis/recombination study of the membranes of Escherichia coli containing either wild type cytochrome bd or inactive E445A mutant was performed using nanosecond absorption spectroscopy. We compared photoinduced changes of heme d-CO complex in one-electron-reduced, two-electron-reduced, and fully-reduced states of cytochromes bd. The line shape of spectra of photodissociation of one-electron-reduced and two-electron-reduced enzymes is strikingly different from that of the fully-reduced enzyme. The difference demonstrates that in the fully-reduced enzyme photolysis of CO from heme d perturbs ferrous heme b595 causing loss of an absorption band centered at 435 nm, thus supporting interactions between heme b595 and heme d in the di-heme oxygen-reducing site, in agreement with previous works. Photolyzed CO recombines with the fully-reduced enzyme monoexponentially with τ ~12 µs, whereas recombination of CO with one-electron-reduced cytochrome bd shows three kinetic phases, with τ ~14 ns, 14 µs, and 280 µs. The spectra of the absorption changes associated with these components are different in line shape. The 14 ns phase, absent in the fully-reduced enzyme, reflects geminate recombination of CO with part of heme d. The 14 µs component reflects bimolecular recombination of CO with heme d and electron backflow from heme d to hemes b in ~4% of the enzyme population. The final, 280 µs component, reflects return of the electron from hemes b to heme d and bimolecular recombination of CO in that population. The fact that even in the two-electron-reduced enzyme, a nanosecond geminate recombination is observed, suggests that namely the redox state of heme b595, and not that of heme b558, controls the pathway(s) by which CO migrates between heme d and the medium.

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“…Stock solutions of NO• (Air Liquide) were prepared by equilibrating degassed water with the NO• pure gas at 1 atm at room temperature yielding 2 mM NO• in solution. Cytochrome bd from E. coli strain GO105/pTK1 was isolated as reported [63,64]. The purified enzyme displayed high oxidase activity (see below) and characteristic absorption spectra both 'as prepared' and after dithionite reduction (not shown).…”

Section: Reagents and Enzyme Purificationmentioning

confidence: 99%

Cytochrome bd from Escherichia coli catalyzes peroxynitrite decomposition

Borisov

Forte

Siletsky

et al. 2015

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Cytochrome bd is a prokaryotic respiratory quinol oxidase phylogenetically unrelated to heme-copper oxidases, that was found to promote virulence in some bacterial pathogens. Cytochrome bd from Escherichia coli was previously reported to contribute not only to proton motive force generation, but also to bacterial resistance to nitric oxide (NO) and hydrogen peroxide (H2O2). Here, we investigated the interaction of the purified enzyme with peroxynitrite (ONOO(-)), another harmful reactive species produced by the host to kill invading microorganisms. We found that addition of ONOO(-) to cytochrome bd in turnover with ascorbate and N,N,N',N'-tetramethyl-p-phenylenediamine (TMPD) causes the irreversible inhibition of a small (≤15%) protein fraction, due to the NO generated from ONOO(-) and not to ONOO(-) itself. Consistently, addition of ONOO(-) to cells of the E. coli strain GO105/pTK1, expressing cytochrome bd as the only terminal oxidase, caused only a minor (≤5%) irreversible inhibition of O2 consumption, without measurable release of NO. Furthermore, by directly monitoring the kinetics of ONOO(-) decomposition by stopped-flow absorption spectroscopy, it was found that the purified E. coli cytochrome bd in turnover with O2 is able to metabolize ONOO(-) with an apparent turnover rate as high as ~10 mol ONOO(-) (mol enzyme)(-1) s(-1) at 25°C. To the best of our knowledge, this is the first time that the kinetics of ONOO(-) decomposition by a terminal oxidase has been investigated. These results strongly suggest a protective role of cytochrome bd against ONOO(-) damage.

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Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: Heme d binds CO with high affinity

Cited by 49 publications

References 79 publications

Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer

Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer

Heme–heme and heme–ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy

Cytochrome bd from Escherichia coli catalyzes peroxynitrite decomposition

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