Structural alterations in a component of cytochrome c oxidase and molecular evolution of pathogenic Neisseria in humans.

Structural alterations in a component of cytochrome c oxidase and molecular evolution of pathogenic Neisseria in humans.
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DOI:
10.1371/journal.ppat.1001055
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发表时间:
2010-08-19
期刊:
影响因子:
6.7
通讯作者:
Koomey M
Koomey M
中科院分区:
医学1区
文献类型:
--
作者:
Aspholm M;Aas FE;Harrison OB;Quinn D;Vik A;Viburiene R;Tønjum T;Moir J;Maiden MC;Koomey M

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Three closely related bacterial species within the genus Neisseria are of importance to human disease and health. Neisseria meningitidis is a major cause of meningitis, while Neisseria gonorrhoeae is the agent of the sexually transmitted disease gonorrhea and Neisseria lactamica is a common, harmless commensal of children. Comparative genomics have yet to yield clear insights into which factors dictate the unique host-parasite relationships exhibited by each since, as a group, they display remarkable conservation at the levels of nucleotide sequence, gene content and synteny. Here, we discovered two rare alterations in the gene encoding the CcoP protein component of cytochrome cbb 3 oxidase that are phylogenetically informative. One is a single nucleotide polymorphism resulting in CcoP truncation that acts as a molecular signature for the species N. meningitidis. We go on to show that the ancestral ccoP gene arose by a unique gene duplication and fusion event and is specifically and completely distributed within species of the genus Neisseria. Surprisingly, we found that strains engineered to express either of the two CcoP forms conditionally differed in their capacity to support nitrite-dependent, microaerobic growth mediated by NirK, a nitrite reductase. Thus, we propose that changes in CcoP domain architecture and ensuing alterations in function are key traits in successive, adaptive radiations within these metapopulations. These findings provide a dramatic example of how rare changes in core metabolic proteins can be connected to significant macroevolutionary shifts. They also show how evolutionary change at the molecular level can be linked to metabolic innovation and its reversal as well as demonstrating how genotype can be used to infer alterations of the fitness landscape within a single host. The closely related bacterial species N. meningitidis, N. gonorrhoeae and N. lactamica exclusively colonise mucosal surfaces in humans. While N. gonorrhoeae leads to gonorrhea, the other two species persist mainly in their host in the absence of disease. N. meningitidis does occasionally cause severe, life threatening illness, however. Little is known about the factors and elements that dictate the unique human interactions exhibited by each species. Moreover, the evolutionary relationships between these species are poorly characterized. Here, we describe two successive alterations in a single gene that can be linked first to all species within the genus Neisseria and then the species N. meningitidis. We also show these signature alterations have phenotypic consequences by affecting core respiratory metabolic processes. These findings have significant implications for the evolution of related bacterial species within a single host and provide a novel perspective on the episodic and reversible nature of innovative adaptation.
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