Abstract
Glucosyltransferases (Gtfs) catalyze the synthesis of glucans from sucrose and are produced by several species of lactic-acid bacteria. The oral bacterium Streptococcus mutans produces large amounts of glucans through the action of three Gtfs. GtfD produces water-soluble glucan (WSG), GtfB synthesizes water-insoluble glucans (WIG) and GtfC produces mainly WIG but also WSG. These enzymes, especially those synthesizing WIG, are of particular interest because of their role in the formation of dental plaque, an environment where S. mutans can thrive and produce lactic acid, promoting the formation of dental caries. We sequenced the gtfB, gtfC and gtfD genes from several mutans streptococcal strains isolated from the oral cavity of humans and searched for their homologues in strains isolated from chimpanzees and macaque monkeys. The sequence data were analyzed in conjunction with the available Gtf sequences from other bacteria in the genera Streptococcus, Lactobacillus and Leuconostoc to gain insights into the evolutionary history of this family of enzymes, with a particular emphasis on S. mutans Gtfs. Our analyses indicate that streptococcal Gtfs arose from a common ancestral progenitor gene, and that they expanded to form two clades according to the type of glucan they synthesize. We also show that the clade of streptococcal Gtfs synthesizing WIG appeared shortly after the divergence of viviparous, dentate mammals, which potentially contributed to the formation of dental plaque and the establishment of several streptococci in the oral cavity. The two S. mutans Gtfs capable of WIG synthesis, GtfB and GtfC, are likely the product of a gene duplication event. We dated this event to coincide with the divergence of the genomes of ancestral early primates. Thus, the acquisition and diversification of S. mutans Gtfs predates modern humans and is unrelated to the increase in dietary sucrose consumption.
Highlights
Streptococcus mutans is a member of the indigenous human oral biota, of worldwide distribution [1]
Water-soluble glucans (WSG), known as dextran, are rich in a-1,6 glucosidic linkages, while a higher content of a-1,3 glucosidic linkages is characteristic of waterinsoluble glucans (WIG), known as mutan [9]
The phylogenetic relationships between S. macacae, S. troglodytae and S. mutans GtfB and GtfC were not resolved with this approach
Summary
Streptococcus mutans is a member of the indigenous human oral biota, of worldwide distribution [1]. It largely contributes to the formation of the biofilm known as dental plaque through the production of extracellular glucans from dietary sucrose. Glucans mediate the attachment of bacteria to the tooth surface [2,3] and to other members of the oral biota [4,5], promoting biofilm development. In this environment S. mutans produces mainly lactic acid as the byproduct of the metabolism of sucrose and other carbohydrates. Glucans are high molecular weight D-glucose polymers synthesized by extracellular enzymes called glucosyltransferases (more generally known as glucansucrases, EC 2.4.1.5). Water-soluble glucans (WSG), known as dextran, are rich in a-1,6 glucosidic linkages, while a higher content of a-1,3 glucosidic linkages is characteristic of waterinsoluble glucans (WIG), known as mutan [9]
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