Abstract
ABSTRACTCommunication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence. This is achieved by the secretion and detection of small signaling molecules called autoinducers, a process termed quorum sensing. To date, the only signaling molecule recognized by both Gram-positive and Gram-negative bacteria is autoinducer 2 (AI-2), synthesized by the metabolic enzyme LuxS (S-ribosylhomocysteine lyase) as a by-product of the activated methyl cycle. Homologues of LuxS are ubiquitous in bacteria, suggesting a key role in interspecies, as well as intraspecies, communication. Gram-negative bacteria sense and respond to AI-2 via the Lsr ABC transporter system or by the LuxP/LuxQ phosphorelay system. However, homologues of these systems are absent from Gram-positive bacteria and the AI-2 receptor is unknown. Here we show that in the major human pathogen Streptococcus pneumoniae, sensing of exogenous AI-2 is dependent on FruA, a fructose-specific phosphoenolpyruvate-phosphotransferase system that is highly conserved in Gram-positive pathogens. Importantly, AI-2 signaling via FruA enables the bacterium to utilize galactose as a carbon source and upregulates the Leloir pathway, thereby leading to increased production of capsular polysaccharide and a hypervirulent phenotype.
Highlights
Communication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence
Gram-negative bacteria such as Escherichia coli and Salmonella spp. sense and respond to autoinducer 2 (AI-2) via the Lsr ABC transporter system, while in Vibrio spp., a furanosyl-borate-diester form of AI-2 is detected by the LuxP/LuxQ phosphorelay system [11]
To distinguish between true QS effects mediated by AI-2 from the indirect consequences of luxS disruption on the activated methyl cycle, we examined the capacity of various concentrations of exogenous purified DPD (AI-2) to complement the growth defect of D39ΔluxS in mbio.asm.org 3
Summary
Communication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence. The capacity to form a biofilm on host mucosal surfaces is increasingly being recognized as a critical event in the pathogenesis of pneumococcal disease [4] Within these communities, bacteria exchange both metabolic signals and metabolizable factors, but they can communicate via a series of small diffusible autoinducer (AI) molecules that induce changes in gene expression in target cells in a density-dependent fashion. Gram-negative bacteria such as Escherichia coli and Salmonella spp. sense and respond to AI-2 via the Lsr ABC transporter system, while in Vibrio spp., a furanosyl-borate-diester form of AI-2 is detected by the LuxP/LuxQ phosphorelay system [11] Homologues of these systems are absent from Gram-positive bacteria and the AI-2 receptor is unknown
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