Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae
Date
2010
Authors
Ogunniyi, A.
Mahdi, L.
Jennings, M.
McEwan, A.
McDevitt, C.
Van der Hoek, M.
Bagley, C.
Hoffmann, P.
Gould, K.
Paton, J.
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Journal article
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Journal of Bacteriology, 2010; 192(17):4489-4497
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Abiodun D. Ogunniyi, Layla K. Mahdi, Michael P. Jennings, Alastair G. McEwan, Christopher A. McDevitt, Mark B. Van der Hoek, Christopher J. Bagley, Peter Hoffmann, Katherine A. Gould, and James C. Paton
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Abstract
The importance of Mn2+ for pneumococcal physiology and virulence has been studied extensively. However, the specific cellular role(s) for which Mn2+ is required are yet to be fully elucidated. Here, we analyzed the effect of Mn2+ 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 Mn2+ transporter, pneumococcal surface antigen A (PsaA), with its isogenic wild-type counterpart. We provide clear evidence for the Mn2+-dependent regulation of the expression of oxidative-stress-response enzymes SpxB and Mn2+-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 Mn2+ stress. A significant increase in 6-phosphogluconate dehydrogenase activity in the psaA mutant grown under Mn2+-replete conditions and upregulation of an oligopeptide ABC permease (AppDCBA) were also observed. Together, the results of transcriptomic and proteomic analyses provided evidence for Mn2+ 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 Mn2+ transport by PsaA in pneumococcal competence, physiology, and metabolism and elucidate mechanisms underlying the response to Mn2+ stress.
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Copyright © 2010, American Society for Microbiology. All Rights Reserved.