Carbonic Anhydrase Is Essential forStreptococcus pneumoniaeGrowth in Environmental Ambient Air

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Abstract
The respiratory tract pathogenStreptococcus pneumoniaeneeds to adapt to the different levels of carbon dioxide (CO2) it encounters during transmission, colonization, and infection. Since CO2is important for various cellular processes, factors that allow optimal CO2sequestering are likely to be important for pneumococcal growth and survival. In this study, we showed that the putative pneumococcal carbonic anhydrase (PCA) is essential forin vitrogrowth ofS. pneumoniaeunder the CO2-poor conditions found in environmental ambient air. Enzymatic analysis showed that PCA catalyzes the reversible hydration of CO2to bicarbonate (HCO3−), an essential step to prevent the cellular release of CO2. The addition of unsaturated fatty acids (UFAs) reversed the CO2-dependentin vitrogrowth inhibition ofS. pneumoniaestrains lacking thepcagene (Δpca), indicating that PCA-mediated CO2fixation is at least associated with HCO3−-dependentde novobiosynthesis of UFAs. Besides being necessary for growth in environmental ambient conditions, PCA-mediated CO2fixation pathways appear to be required for intracellular survival in host cells. This effect was especially pronounced during invasion of human brain microvascular endothelial cells (HBMEC) and uptake by murine J774 macrophage cells but not during interaction ofS. pneumoniaewith Detroit 562 pharyngeal epithelial cells. Finally, the highly conservedpcagene was found to be invariably present in both CO2-independent and naturally circulating CO2-dependent strains, suggesting a conserved essential role for PCA and PCA-mediated CO2fixation pathways for pneumococcal growth and survival.

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