Two Gene Clusters Coordinate Galactose and Lactose Metabolism in Streptococcus gordonii

Abstract

ABSTRACTStreptococcus gordoniiis an early colonizer of the human oral cavity and an abundant constituent of oral biofilms. Two tandemly arranged gene clusters, designatedlacandgal, were identified in theS. gordoniiDL1 genome, which encode genes of the tagatose pathway (lacABCD) and sugar phosphotransferase system (PTS) enzyme II permeases. Genes encoding a predicted phospho-β-galactosidase (LacG), a DeoR family transcriptional regulator (LacR), and a transcriptional antiterminator (LacT) were also present in the clusters. Growth and PTS assays supported that the permease designated EIILactransports lactose and galactose, whereas EIIGaltransports galactose. The expression of the gene for EIIGalwas markedly upregulated in cells growing on galactose. Using promoter-catfusions, a role for LacR in the regulation of the expressions of both gene clusters was demonstrated, and thegalcluster was also shown to be sensitive to repression by CcpA. The deletion oflacTcaused an inability to grow on lactose, apparently because of its role in the regulation of the expression of the genes for EIILac, but had little effect on galactose utilization.S. gordoniimaintained a selective advantage overStreptococcus mutansin a mixed-species competition assay, associated with its possession of a high-affinity galactose PTS, althoughS. mutanscould persist better at low pHs. Collectively, these results support the concept that the galactose and lactose systems ofS. gordoniiare subject to complex regulation and that a high-affinity galactose PTS may be advantageous whenS. gordoniiis competing against the caries pathogenS. mutansin oral biofilms.