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Molecular Pathogenesis

Synergy between Nutritional Immunity and Independent Host Defenses Contributes to the Importance of the MntABC Manganese Transporter during Staphylococcus aureus Infection

Jana N. Radin, Jamie Zhu, Erin B. Brazel, Christopher A. McDevitt, Thomas E. Kehl-Fie
Victor J. Torres, Editor
Jana N. Radin
aDepartment of Microbiology, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
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Jamie Zhu
aDepartment of Microbiology, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
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Erin B. Brazel
bResearch Centre for Infectious Diseases, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia
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Christopher A. McDevitt
bResearch Centre for Infectious Diseases, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia
cDepartment of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia
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Thomas E. Kehl-Fie
aDepartment of Microbiology, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
dCarl R. Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
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Victor J. Torres
New York University School of Medicine
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DOI: 10.1128/IAI.00642-18
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ABSTRACT

During infection, the host utilizes a diverse array of processes to combat invaders, including the restriction of availability of essential nutrients such as manganese. Similarly to many other pathogens, Staphylococcus aureus possesses two manganese importers, MntH and MntABC. Several infection models have revealed a critical role for MntABC during staphylococcal infection. However, culture-based studies have suggested parity between the two transporters when cells are resisting manganese starvation imposed by the manganese binding immune effector calprotectin. In this investigation, initial elemental analysis revealed that MntABC is the primary transporter responsible for obtaining manganese in culture in the presence of calprotectin. MntABC was also necessary to maintain wild-type levels of manganese-dependent superoxide dismutase activity in the presence of calprotectin. Building on this framework, we investigated if MntABC enabled S. aureus to resist the synergistic actions of nutritional immunity and other host defenses. This analysis revealed that MntABC critically contributes to staphylococcal growth when S. aureus is subjected to manganese limitations and exposed to oxidative stress. This transporter was also important for growth in manganese-limited environments when S. aureus was forced to consume glucose as an energy source, which occurs when it encounters nitric oxide. MntABC also expanded the pH range conducive for S. aureus growth under conditions of manganese scarcity. Collectively, the data presented in this work provide a robust molecular basis for the crucial role of MntABC in staphylococcal virulence. Further, this work highlights the importance of synergy between host defenses and the necessity of evaluating the contribution of virulence factors to pathogenesis in the presence of multiple stressors.

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Synergy between Nutritional Immunity and Independent Host Defenses Contributes to the Importance of the MntABC Manganese Transporter during Staphylococcus aureus Infection
Jana N. Radin, Jamie Zhu, Erin B. Brazel, Christopher A. McDevitt, Thomas E. Kehl-Fie
Infection and Immunity Dec 2018, 87 (1) e00642-18; DOI: 10.1128/IAI.00642-18

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Synergy between Nutritional Immunity and Independent Host Defenses Contributes to the Importance of the MntABC Manganese Transporter during Staphylococcus aureus Infection
Jana N. Radin, Jamie Zhu, Erin B. Brazel, Christopher A. McDevitt, Thomas E. Kehl-Fie
Infection and Immunity Dec 2018, 87 (1) e00642-18; DOI: 10.1128/IAI.00642-18
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KEYWORDS

ABC transporters
calprotectin
infection
manganese
MntABC
MntH
nutritional immunity
Staphylococcus aureus

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