Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>

ABSTRACT Early epidemiological studies implicated manganese (Mn) as a possible caries-promoting agent, while laboratory studies have indicated that manganese stimulates the expression of virulence-related factors in the dental pathogen Streptococcus mutans. To better understand the importance of man...

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Autores principales:	Jessica K. Kajfasz, Callahan Katrak, Tridib Ganguly, Jonathan Vargas, Logan Wright, Zachary T. Peters, Grace A. Spatafora, Jacqueline Abranches, José A. Lemos
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	S. mutans manganese metal transport stress response dental caries biofilm Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4a39beab002143eab65b05a5c7e26630
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spelling	oai:doaj.org-article:4a39beab002143eab65b05a5c7e266302021-11-15T15:27:52ZManganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>10.1128/mSphere.00764-192379-5042https://doaj.org/article/4a39beab002143eab65b05a5c7e266302020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00764-19https://doaj.org/toc/2379-5042ABSTRACT Early epidemiological studies implicated manganese (Mn) as a possible caries-promoting agent, while laboratory studies have indicated that manganese stimulates the expression of virulence-related factors in the dental pathogen Streptococcus mutans. To better understand the importance of manganese homeostasis to S. mutans pathophysiology, we first used RNA sequencing to obtain the global transcriptional profile of S. mutans UA159 grown under Mn-restricted conditions. Among the most highly expressed genes were those of the entire sloABC operon, encoding a dual iron/manganese transporter, and an uncharacterized gene, here mntH, that codes for a protein bearing strong similarity to Nramp-type transporters. While inactivation of sloC, which encodes the lipoprotein receptor of the SloABC system, or of mntH alone had no major consequence for the overall fitness of S. mutans, simultaneous inactivation of sloC and mntH (ΔsloC ΔmntH) impaired growth and survival under Mn-restricted conditions, including in human saliva or in the presence of calprotectin. Further, disruption of Mn transport resulted in diminished stress tolerance and reduced biofilm formation in the presence of sucrose. These phenotypes were markedly improved when cells were provided with excess Mn. Metal quantifications revealed that the single mutant strains contained intracellular levels of Mn similar to those seen with the parent strain, whereas Mn was nearly undetectable in the ΔsloC ΔmntH strain. Collectively, these results reveal that SloABC and MntH work independently and cooperatively to promote cell growth under Mn-restricted conditions and that maintenance of Mn homeostasis is essential for the expression of major virulence attributes in S. mutans. IMPORTANCE As transition biometals such as manganese (Mn) are essential for all forms of life, the ability to scavenge biometals in the metal-restricted host environment is an important trait of successful cariogenic pathobionts. Here, we showed that the caries pathogen Streptococcus mutans utilizes two Mn transport systems, namely, SloABC and MntH, to acquire Mn from the environment and that the ability to maintain the cellular levels of Mn is important for the manifestation of characteristics that associate S. mutans with dental caries. Our results indicate that the development of strategies to deprive S. mutans of Mn hold promise in the combat against this important bacterial pathogen.Jessica K. KajfaszCallahan KatrakTridib GangulyJonathan VargasLogan WrightZachary T. PetersGrace A. SpataforaJacqueline AbranchesJosé A. LemosAmerican Society for MicrobiologyarticleS. mutansmanganesemetal transportstress responsedental cariesbiofilmMicrobiologyQR1-502ENmSphere, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	S. mutans manganese metal transport stress response dental caries biofilm Microbiology QR1-502
spellingShingle	S. mutans manganese metal transport stress response dental caries biofilm Microbiology QR1-502 Jessica K. Kajfasz Callahan Katrak Tridib Ganguly Jonathan Vargas Logan Wright Zachary T. Peters Grace A. Spatafora Jacqueline Abranches José A. Lemos Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
description	ABSTRACT Early epidemiological studies implicated manganese (Mn) as a possible caries-promoting agent, while laboratory studies have indicated that manganese stimulates the expression of virulence-related factors in the dental pathogen Streptococcus mutans. To better understand the importance of manganese homeostasis to S. mutans pathophysiology, we first used RNA sequencing to obtain the global transcriptional profile of S. mutans UA159 grown under Mn-restricted conditions. Among the most highly expressed genes were those of the entire sloABC operon, encoding a dual iron/manganese transporter, and an uncharacterized gene, here mntH, that codes for a protein bearing strong similarity to Nramp-type transporters. While inactivation of sloC, which encodes the lipoprotein receptor of the SloABC system, or of mntH alone had no major consequence for the overall fitness of S. mutans, simultaneous inactivation of sloC and mntH (ΔsloC ΔmntH) impaired growth and survival under Mn-restricted conditions, including in human saliva or in the presence of calprotectin. Further, disruption of Mn transport resulted in diminished stress tolerance and reduced biofilm formation in the presence of sucrose. These phenotypes were markedly improved when cells were provided with excess Mn. Metal quantifications revealed that the single mutant strains contained intracellular levels of Mn similar to those seen with the parent strain, whereas Mn was nearly undetectable in the ΔsloC ΔmntH strain. Collectively, these results reveal that SloABC and MntH work independently and cooperatively to promote cell growth under Mn-restricted conditions and that maintenance of Mn homeostasis is essential for the expression of major virulence attributes in S. mutans. IMPORTANCE As transition biometals such as manganese (Mn) are essential for all forms of life, the ability to scavenge biometals in the metal-restricted host environment is an important trait of successful cariogenic pathobionts. Here, we showed that the caries pathogen Streptococcus mutans utilizes two Mn transport systems, namely, SloABC and MntH, to acquire Mn from the environment and that the ability to maintain the cellular levels of Mn is important for the manifestation of characteristics that associate S. mutans with dental caries. Our results indicate that the development of strategies to deprive S. mutans of Mn hold promise in the combat against this important bacterial pathogen.
format	article
author	Jessica K. Kajfasz Callahan Katrak Tridib Ganguly Jonathan Vargas Logan Wright Zachary T. Peters Grace A. Spatafora Jacqueline Abranches José A. Lemos
author_facet	Jessica K. Kajfasz Callahan Katrak Tridib Ganguly Jonathan Vargas Logan Wright Zachary T. Peters Grace A. Spatafora Jacqueline Abranches José A. Lemos
author_sort	Jessica K. Kajfasz
title	Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
title_short	Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
title_full	Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
title_fullStr	Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
title_full_unstemmed	Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>
title_sort	manganese uptake, mediated by sloabc and mnth, is essential for the fitness of <named-content content-type="genus-species">streptococcus mutans</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/4a39beab002143eab65b05a5c7e26630
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Manganese Uptake, Mediated by SloABC and MntH, Is Essential for the Fitness of <named-content content-type="genus-species">Streptococcus mutans</named-content>

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