Trk2 Potassium Transport System in Streptococcus mutans and Its Role in Potassium Homeostasis, Biofilm Formation, and Stress Tolerance

Abstract

ABSTRACT Potassium (K + ) is the most abundant cation in the fluids of dental biofilm. The biochemical and biophysical functions of K + and a variety of K + transport systems have been studied for most pathogenic bacteria but not for oral pathogens. In this study, we establish the modes of K + acquisition in Streptococcus mutans and the importance of K + homeostasis for its virulence attributes. The S. mutans genome harbors four putative K + transport systems that included two Trk-like transporters (designated Trk1 and Trk2), one glutamate/K + cotransporter (GlnQHMP), and a channel-like K + transport system (Kch). Mutants lacking Trk2 had significantly impaired growth, acidogenicity, aciduricity, and biofilm formation. [K + ] less than 5 mM eliminated biofilm formation in S. mutans . The functionality of the Trk2 system was confirmed by complementing an Escherichia coli TK2420 mutant strain, which resulted in significant K + accumulation, improved growth, and survival under stress. Taken together, these results suggest that Trk2 is the main facet of the K + -dependent cellular response of S. mutans to environment stresses. IMPORTANCE Biofilm formation and stress tolerance are important virulence properties of caries-causing Streptococcus mutans . To limit these properties of this bacterium, it is imperative to understand its survival mechanisms. Potassium is the most abundant cation in dental plaque, the natural environment of S. mutans . K + is known to function in stress tolerance, and bacteria have specialized mechanisms for its uptake. However, there are no reports to identify or characterize specific K + transporters in S. mutans . We identified the most important system for K + homeostasis and its role in the biofilm formation, stress tolerance, and growth. We also show the requirement of environmental K + for the activity of biofilm-forming enzymes, which explains why such high levels of K + would favor biofilm formation.