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A Unique Reverse Adaptation Mechanism Assists Bordetella pertussis in Resistance to Both Scarcity and Toxicity of Manganese
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SYSNO ASEP 0547696 Druh ASEP J - Článek v odborném periodiku Zařazení RIV J - Článek v odborném periodiku Poddruh J Článek ve WOS Název A Unique Reverse Adaptation Mechanism Assists Bordetella pertussis in Resistance to Both Scarcity and Toxicity of Manganese Tvůrce(i) Čapek, Jan (MBU-M) ORCID
Procházková, Ilona (MBU-M)
Matoušek, Tomáš (UIACH-O) RID, ORCID
Hot, D. (FR)
Večerek, Branislav (MBU-M) RID, ORCIDČíslo článku e0190221 Zdroj.dok. mBio. - : American Society for Microbiology - ISSN 2161-2129
Roč. 12, č. 5 (2021)Poč.str. 14 s. Jazyk dok. eng - angličtina Země vyd. US - Spojené státy americké Klíč. slova Bordetella ; Bordetella pertussis ; genome decay ; manganese ; oxidative stress ; pathogen adaptation Vědní obor RIV EE - Mikrobiologie, virologie Obor OECD Microbiology Vědní obor RIV – spolupráce Ústav analytické chemie - Analytická chemie, separace CEP GA19-12338S GA ČR - Grantová agentura ČR Způsob publikování Open access Institucionální podpora MBU-M - RVO:61388971 ; UIACH-O - RVO:68081715 UT WOS 000735254700004 EID SCOPUS 85120926442 DOI 10.1128/mBio.01902-21 Anotace The ability of bacterial pathogens to acquire essential micronutrients is critical for their survival in the host environment. Manganese plays a complex role in the virulence of a variety of pathogens due to its function as an antioxidant and enzymatic cofactor. Therefore, host cells deprive pathogens of manganese to prevent or attenuate infection. Here, we show that evolution of the human-restricted pathogen Bordetella pertussis has selected for an inhibitory duplication within a manganese exporter of the calcium:cation antiporter superfamily. Intriguingly, upon exposure to toxic levels of manganese, the nonfunctional exporter becomes operative in resister cells due to a unique reverse adaptation mechanism. However, compared with wild-type (wt) cells, the resisters carrying a functional copy of the exporter displayed strongly reduced intracellular levels of manganese and impaired growth under oxidative stress. Apparently, inactivation of the manganese exporter and the resulting accumulation of manganese in the cytosol benefited the pathogen by improving its survival under stress conditions. The inhibitory duplication within the exporter gene is highly conserved among B. pertussis strains, absent from all other Bordetella species and from a vast majority of organisms across all kingdoms of life. Therefore, we conclude that inactivation of the exporter gene represents an exceptional example of a flexible genome decay strategy employed by a human pathogen to adapt to its exclusive host. IMPORTANCE Bordetella pertussis, a respiratory pathogen restricted to humans, continuously adapts its genome to its exclusive host. We show that speciation of this reemerging pathogen was accompanied by loss of function of the manganese exporter. Intriguingly, the functionality of the exporter can be restored in the presence of toxic levels of manganese by a unique genetic modification. Pracoviště Mikrobiologický ústav Kontakt Eliška Spurná, eliska.spurna@biomed.cas.cz, Tel.: 241 062 231 Rok sběru 2022 Elektronická adresa https://pubmed.ncbi.nlm.nih.gov/34700381/
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