Central role of manganese in regulation of stress responses, physiology, and metabolism in streptococcus pneumoniae

Article


Ogunniyi, Abiodun D., Mahdi, Layla K., Jennings, Michael P., McEwan, Alastair G., McDevitt, Christopher A., Van der Hoek, Mark B., Bagley, Christopher J., Hoffmann, Peter, Gould, Katherine A. and Paton, James C.. 2010. "Central role of manganese in regulation of stress responses, physiology, and metabolism in streptococcus pneumoniae." Journal of Bacteriology. 192 (17), pp. 4489-4497. https://doi.org/10.1128/JB.00064-10
Article Title

Central role of manganese in regulation of stress responses, physiology, and metabolism in streptococcus pneumoniae

ERA Journal ID2483
Article CategoryArticle
AuthorsOgunniyi, Abiodun D. (Author), Mahdi, Layla K. (Author), Jennings, Michael P. (Author), McEwan, Alastair G. (Author), McDevitt, Christopher A. (Author), Van der Hoek, Mark B. (Author), Bagley, Christopher J. (Author), Hoffmann, Peter (Author), Gould, Katherine A. (Author) and Paton, James C. (Author)
Journal TitleJournal of Bacteriology
Journal Citation192 (17), pp. 4489-4497
Number of Pages9
Year2010
PublisherAmerican Society for Microbiology
Place of PublicationUnited States
ISSN0021-9193
1067-8832
1098-5530
Digital Object Identifier (DOI)https://doi.org/10.1128/JB.00064-10
Web Address (URL)https://journals.asm.org/doi/10.1128/JB.00064-10
Abstract

The importance of Mn(2+) for pneumococcal physiology and virulence has been studied extensively. However, the specific cellular role(s) for which Mn(2+) is required are yet to be fully elucidated. Here, we analyzed the effect of Mn(2+) limitation on the transcriptome and proteome of Streptococcus pneumoniae D39. This was carried out by comparing a deletion mutant lacking the solute binding protein of the high-affinity Mn(2+) transporter, pneumococcal surface antigen A (PsaA), with its isogenic wild-type counterpart. We provide clear evidence for the Mn(2+)-dependent regulation of the expression of oxidative-stress-response enzymes SpxB and Mn(2+)-SodA and virulence-associated genes pcpA and prtA. We also demonstrate the upregulation of at least one oxidative- and nitrosative-stress-response gene cluster, comprising adhC, nmlR, and czcD, in response to Mn(2+) stress. A significant increase in 6-phosphogluconate dehydrogenase activity in the psaA mutant grown under Mn(2+) replete conditions and upregulation of an oligopeptide ABC permease (AppDCBA) were also observed. Together, the results of transcriptomic and proteomic analyses provided evidence for Mn(2+) having a central role in activating or stimulating enzymes involved in central carbon and general metabolism. Our results also highlight the importance of high-affinity Mn(2+) transport by PsaA in pneumococcal competence, physiology, and metabolism and elucidate mechanisms underlying the response to Mn(2+) stress.

KeywordsABC permease; bacterial antigen; gene product; manganese; oligopeptide; permease; phosphogluconate dehydrogenase; pneumococcal surface antigen A; protein soda; protein SpxB; proteome; transcriptome; unclassified drug; adhesion; bacterial protein; lipoprotein; manganese; proteome; PsaA protein; Streptococcus
ANZSRC Field of Research 2020310701. Bacteriology
320701. Medical bacteriology
310109. Proteomics and intermolecular interactions (excl. medical proteomics)
Byline AffiliationsUniversity of Adelaide
Griffith University
University of Queensland
University of London, United Kingdom
Institution of OriginUniversity of Southern Queensland
Funding source
NHMRC
Grant ID
284214
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