TY - JOUR
T1 - Cytochrome c-based domain modularity governs genus-level diversification of electron transfer to dissimilatory nitrite reduction
AU - Aas, Finn Erik
AU - Li, Xi
AU - Edwards, James
AU - Hongrø Solbakken, Monica
AU - Deeudom, Manu
AU - Vik, Åshild
AU - Moir, James
AU - Koomey, Michael
AU - Aspholm, Marina
PY - 2015/12/11
Y1 - 2015/12/11
N2 - 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.weaveriiNirK 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.
AB - 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.weaveriiNirK 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.
UR - http://www.scopus.com/inward/record.url?scp=84931561403&partnerID=8YFLogxK
U2 - 10.1111/1462-2920.12661
DO - 10.1111/1462-2920.12661
M3 - Article
AN - SCOPUS:84931561403
SN - 1462-2912
VL - 17
SP - 2114
EP - 2132
JO - Environmental Microbiology
JF - Environmental Microbiology
IS - 6
ER -