Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria

Abstract

Recent phylogenetic analyses have established that the Epsilonproteobacteria form a globally ubiquitous group of ecologically significant organisms that comprises a diverse range of free-living bacteria as well as host-associated organisms like Wolinella succinogenes and pathogenic Campylobacter and Helicobacter species. Many Epsilonproteobacteria reduce nitrate and nitrite and perform either respiratory nitrate ammonification or denitrification. The inventory of epsilonproteobacterial genomes from 21 different species was analysed with respect to key enzymes involved in respiratory nitrogen metabolism. Most ammonifying Epsilonproteobacteria employ two enzymic electron transport systems named Nap (periplasmic nitrate reductase) and Nrf (periplasmic cytochrome c nitrite reductase). The current knowledge on the architecture and function of the corresponding proton motive force-generating respiratory chains using low-potential electron donors are reviewed in this article and the role of membrane-bound quinone/quinol-reactive proteins (NapH and NrfH) that are representative of widespread bacterial electron transport modules is highlighted. Notably, all Epsilonproteobacteria lack a napC gene in their nap gene clusters. Possible roles of the Nap and Nrf systems in anabolism and nitrosative stress defence are also discussed. Free-living denitrifying Epsilonproteobacteria lack the Nrf system but encode cytochrome cd(1) nitrite reductase, at least one nitric oxide reductase and a characteristic cytochrome c nitrous oxide reductase system (cNosZ). Interestingly, cNosZ is also found in some ammonifying Epsilonproteobacteria and enables nitrous oxide respiration in W. succinogenes.

Disruption of the Termite Gut Microbiota and Its Prolonged Consequences for Fitness

“…Reproductive parameters were compared between treatments using a nonparametric Mann-Whitney U test. (38,46). Thus, further work is required to associate the fitness cost in treated termites with a shift in the ability to use nitrogen.…”

Production and consumption of nitrous oxide in nitrate-ammonifying Wolinella succinogenes cells

“…The epsilonproteobacterium W. succinogenes is a versatile respiratory rumen bacterium that typically uses hydrogen gas or formate as electron donor combined with a multitude of electron donor substrates such as nitrate, nitrite, sulfite, polysulfide and fumarate (Kröger et al, 2002;Kern & Simon, 2009;Kern et al, 2011a;Simon & Kroneck, 2013). The cells stoichiometrically produce ammonium from both nitrate and nitrite and the corresponding cell yields (normalized on the basis of formate consumption) were found to be similar using either of these terminal electron acceptors (Bokranz et al, 1983).…”

“…The respective organisms reduce nitrate to nitrite using a membrane-bound nitrate reductase (Nar) and/or a periplasmic nitrate reductase (Nap) (Richardson et al, 2001;Kern & Simon, 2009;Simon & Klotz, 2013). Prominent examples are Gamma-, Deltaand Epsilonproteobacteria such as Escherichia coli, Salmonella enterica serovar Typhimurium, Shewanella oneidensis, Anaeromyxobacter dehalogenans and Wolinella succinogenes.…”

“…Prominent examples are Gamma-, Deltaand Epsilonproteobacteria such as Escherichia coli, Salmonella enterica serovar Typhimurium, Shewanella oneidensis, Anaeromyxobacter dehalogenans and Wolinella succinogenes. Subsequently, nitrite is reduced to ammonium by cytochrome c nitrite reductase (NrfA), which obtains electrons from the quinone/quinol pool through several different electron transport redox enzyme systems, depending on the organism (Simon, 2002;Kern & Simon, 2009;Simon & Klotz, 2013). Many NrfA-containing ammonifiers that also reduce N 2 O encode cNosZ, for example W. succinogenes, Campylobacter fetus, Desulfitobacterium dehalogenans and A. dehalogenans (Payne et al, 1982;Kern & Simon, 2009;Sanford et al, 2012).…”

Epithelial Coculture and l -Lactate Promote Growth of Helicobacter cinaedi under H 2 -Free Aerobic Conditions

“…5. Nap class enzymes are distinct from Nar class nitrate reductases that generate a proton motive force in various proteobacteria as alternate terminal electron acceptors (Nap enzymes are notably absent from the epsilonproteobacterial subdivision) (43). Nevertheless, periplasmic nitrate reductases may still participate indirectly in anaerobic respiration, as well as other processes in dissimilitatory nitrogen metabolism (44)(45)(46).…”