title: Cytochrome c-based domain modularity governs genus-level diversification of electron transfer to dissimilatory nitrite reduction.
abstract: The genus Neisseria contains two pathogenic species (N. meningitidis and N. gonorrhoeae) in addition to a number of commensal species that primarily colonize mucosal surfaces in man. Within the genus, there is considerable diversity and apparent redundancy in the components involved in respiration. Here, we identify a unique c-type cytochrome (cN ) that is broadly distributed among commensal Neisseria, but absent in the pathogenic species. Specifically, cN supports nitrite reduction in N. gonorrhoeae strains lacking the cytochromes c5 and CcoP established to be critical to NirK nitrite reductase activity. The c-type cytochrome domain of cN shares high sequence identity with those localized c-terminally in c5 and CcoP and all three domains were shown to donate electrons directly to NirK. Thus, we identify three distinct but paralogous proteins that donate electrons to NirK. We also demonstrate functionality for a N. weaverii NirK variant with a C-terminal c-type heme extension. Taken together, modular domain distribution and gene rearrangement events related to these respiratory electron carriers within Neisseria are concordant with major transitions in the macroevolutionary history of the genus. This work emphasizes the importance of denitrification as a selectable trait that may influence speciation and adaptive diversification within this largely host-restricted bacterial genus.
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, N-0316, Norway.
authors.forename: Finn Erik
authors.initials: FE
authors.lastname: Aas
authors.affiliation: Department of Biology, University of York, York, YO10 5DD, UK.
authors.forename: Xi
authors.initials: X
authors.lastname: Li
authors.affiliation: Department of Biology, University of York, York, YO10 5DD, UK.
authors.forename: James
authors.initials: J
authors.lastname: Edwards
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, N-0316, Norway.|Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, N-0316, Norway.
authors.forename: Monica
authors.initials: M
authors.lastname: Hongrø Solbakken
authors.affiliation: Department of Biology, University of York, York, YO10 5DD, UK.|Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand.
authors.forename: Manu
authors.initials: M
authors.lastname: Deeudom
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, N-0316, Norway.
authors.forename: Åshild
authors.initials: Å
authors.lastname: Vik
authors.affiliation: Department of Biology, University of York, York, YO10 5DD, UK.
authors.forename: James
authors.initials: J
authors.lastname: Moir
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, N-0316, Norway.|Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, N-0316, Norway.
authors.forename: Michael
authors.initials: M
authors.lastname: Koomey
authors.affiliation: Department of Biosciences, University of Oslo, Oslo, N-0316, Norway.
authors.forename: Marina
authors.initials: M
authors.lastname: Aspholm
mesh_terms: D000595:Amino Acid Sequence; D019069:Cell Respiration; D045304:Cytochromes c / Q000378:metabolism*; D058440:Denitrification; D004579:Electron Transport; D008969:Molecular Sequence Data; D042805:Neisseria elongata / Q000378:metabolism*; D009344:Neisseria gonorrhoeae / Q000378:metabolism*; D009345:Neisseria meningitidis / Q000378:metabolism*; D009573:Nitrites / Q000378:metabolism*; D010084:Oxidation-Reduction; D017434:Protein Structure, Tertiary
chemical_list: D009573:Nitrites; D045304:Cytochromes c