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Abstract
Shewanella exhibit a remarkable versatility of respiration, with a diverse array of electron acceptors (EAs). In environments where these bacteria thrive, multiple EAs are usually present. However, we know little about strategies by which these EAs and their interaction affect ecophysiology of Shewanella. In this study, we demonstrate in the model strain, Shewanella oneidensis MR-1, that nitrite, not through nitric oxide to which it may convert, inhibits respiration of fumarate, and probably many other EAs whose reduction depends on quinol dehydrogenase CymA. This is achieved via the repression of cyclic adenosine monophosphate (cAMP) production, a second messenger required for activation of cAMP-receptor protein (Crp) which plays a primary role in regulation of respiration. If nitrite is not promptly removed, intracellular cAMP levels drop, and this impairs Crp activity. As a result, the production of nitrite reductase NrfA, CymA, and fumarate reductase FccA is substantially reduced. In contrast, nitrite can be simultaneously respired with trimethylamine N-oxide, resulting in enhanced biomass.
Highlights
Shewanella oneidensis MR-1 is a Gram-negative facultative anaerobe with remarkable respiration abilities that permit the use of a diverse array of terminal electron acceptors (EAs), including fumarate, nitrate, nitrite, thiosulfate, trimethylamine N-oxide (TMAO), dimethylsulfoxide (DMSO), Fe(III), Mn(III) and (IV), Cr(VI), and U(VI), among others (Fredrickson et al, 2008)
We examined the role of nitrite during anaerobiosis and found that inhibition of growth on fumarate, probably many other CymA-dependent EAs, by nitrite is associated with cyclic adenosine 3,5 -monophosphate
Two mM nitrite facilitates growth most effectively, resulting in an OD600 up to 0.06, which is barely visible (Cruz-Garcia et al, 2007; Gao et al, 2009). To determine whether this poor growth is a result of nitrite toxicity, we measured growth of S. oneidensis on fumarate, DMSO, TMAO, or sulfite in the presence of 2 mM nitrite
Summary
Shewanella oneidensis MR-1 is a Gram-negative facultative anaerobe with remarkable respiration abilities that permit the use of a diverse array of terminal electron acceptors (EAs), including fumarate, nitrate, nitrite, thiosulfate, trimethylamine N-oxide (TMAO), dimethylsulfoxide (DMSO), Fe(III), Mn(III) and (IV), Cr(VI), and U(VI), among others (Fredrickson et al, 2008). For nitrate and nitrite respiration, most bacteria use the quinol dehydrogenases NapC and NrfBCD (or NrfH) to transfer electrons to the terminal reductases NapA and NrfA, respectively. The role of CymA could be partially, but significantly less effectively, fulfilled by the bc complex and SirCD, which primarily function as quinol dehydrogenases to transport electrons to the cytochrome cbb oxidase and to sulfite reductase, respectively (Cordova et al, 2011; Zhou et al, 2013; Fu et al, 2014). One consequence of sharing CymA is that reduction of Impacts of Nitrite in S. oneidensis nitrite to ammonium by NrfA does not commence until nitrate is thoroughly exhausted, resulting in a characteristic two-step reduction of nitrate (Gao et al, 2009)
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