Identification of a conserved GNAT-family lysine acetyltransferase in Streptococcus gordonii involved in biofilm formation and oral colonization

Abstract

ABSTRACT Streptococcus gordonii is a gram-positive oral bacterium capable of adhering to a variety of biotic and abiotic surfaces and forming biofilms. To characterize physiological changes associated with biofilm formation in S. gordonii, we investigated the roles of two putative GCN5-related N-acetyltransferases (GNATs), SGO_2030 and SGO_2031, in in vitro biofilm formation on saliva-coated surfaces using the laboratory strain DL1. Our results demonstrate that SGO_2031, but not SGO_2030, seems to contribute to biofilm formation by modulating the abundance of extracellular polysaccharides within the biofilm matrix. This defect in biofilm formation observed by the deletion of SGO_2031 resulted in a significant fitness disadvantage during colonization of the murine oral cavity compared to the wild-type parent strain. Consistent with the role of S. gordonii as an early colonizer of tooth surfaces that influences oral biofilm community structure, inoculation with either the wild-type or the SGO_2031 mutant strain led to distinct alterations in the murine oral microbiome composition. Deletion of SGO_2031 also resulted in changes in protein acetylation patterns, as assessed by Western immunoblot analysis, supporting the role of this enzyme as an acetyltransferase. Given that SGO_2031 is conserved and widely distributed among streptococci, we propose naming this enzyme Streptococcal Lysine Acetyltransferase A (SktA). IMPORTANCE Protein acetylation is a common posttranslational modification conserved across all domains of life. In bacteria, protein acetylation is carried out by homologs of the GCN5-related N-acetyltransferase (GNAT) family. GNATs catalyze the transfer of an acetyl group from acetyl-CoA to the ε-amino group of lysine residues on proteins. This process changes the charge and length of lysine residues, resulting in changes to protein function. Streptococcus gordonii is predicted to encode 17 GNAT homologs. Here, we report that one of them, SGO_2031 (SktA), plays an important role in S. gordonii biofilms. Protein acetylation is a common posttranslational modification conserved across all domains of life. In bacteria, protein acetylation is carried out by homologs of the GCN5-related N-acetyltransferase (GNAT) family. GNATs catalyze the transfer of an acetyl group from acetyl-CoA to the ε-amino group of lysine residues on proteins. This process changes the charge and length of lysine residues, resulting in changes to protein function. Streptococcus gordonii is predicted to encode 17 GNAT homologs. Here, we report that one of them, SGO_2031 (SktA), plays an important role in S. gordonii biofilms.