Cytochrome c‐based domain modularity governs genus‐level diversification of electron transfer to dissimilatory nitrite reduction

FE Aas; J Edwards; Solbakken M Hongrø; M Deeudom; Å Vik; J Moir; M Koomey; M Aspholm; Xi Li

doi:10.1111/1462-2920.12661

Cytochrome c‐based domain modularity governs genus‐level diversification of electron transfer to dissimilatory nitrite reduction

FE Aas, J Edwards, Solbakken M Hongrø, M Deeudom, Å Vik, J Moir, M Koomey, M Aspholm, Xi Li

Peninsula Medical School

University of York

Research output: Contribution to journal › Article › peer-review

Abstract

SummaryThe 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.

Original language	English
Pages (from-to)	2114-2132
Number of pages	0
Journal	Environmental Microbiology
Volume	17
Issue number	6
Early online date	11 Dec 2014
DOIs	https://doi.org/10.1111/1462-2920.12661
Publication status	Published - Jun 2015

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@article{c52666a8a2a240de83e95aa5b5b0a34b,

title = "Cytochrome c‐based domain modularity governs genus‐level diversification of electron transfer to dissimilatory nitrite reduction",

abstract = "SummaryThe 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.",

author = "FE Aas and J Edwards and Hongr{\o}, {Solbakken M} and M Deeudom and {\AA} Vik and J Moir and M Koomey and M Aspholm and Xi Li",

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doi = "10.1111/1462-2920.12661",

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T1 - Cytochrome c‐based domain modularity governs genus‐level diversification of electron transfer to dissimilatory nitrite reduction

AU - Aas, FE

AU - Edwards, J

AU - Hongrø, Solbakken M

AU - Deeudom, M

AU - Vik, Å

AU - Moir, J

AU - Koomey, M

AU - Aspholm, M

AU - Li, Xi

PY - 2015/6

Y1 - 2015/6

N2 - SummaryThe 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.

AB - SummaryThe 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.

U2 - 10.1111/1462-2920.12661

DO - 10.1111/1462-2920.12661

M3 - Article

SN - 1462-2912

VL - 17

SP - 2114

EP - 2132

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 6

ER -

Cytochrome c‐based domain modularity governs genus‐level diversification of electron transfer to dissimilatory nitrite reduction

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