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      Evolution of Cariogenic Character in Streptococcus mutans: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes

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      Scientific Reports
      Nature Publishing Group

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          Abstract

          Acquisition of the ability to produce polysaccharides from sucrose, i.e. the gtf gene encoding glucosyltransferase (GTF), is the key evolutionary event enabling dental biofilm formation by streptococci. To clarify the ancestry of streptococcal GTFs, time of its occurrence, and order of specific events, we investigated the distribution of GTFs among bacteria by phylogenetic analysis of the glycosyl hydrolase family 70 enzymes. We found that streptococcal GTFs were derived from other lactic acid bacteria such as Lactobacillus and Leuconostoc, and propose the following evolutionary model: horizontal gene transfer via transposons occurred when streptococci encountered lactic acid bacteria contained in fermented food. Intra-genomic gene duplication occurred by a secondary selection pressure such as consumption of refined sugar. Our findings concerning this evolution in Streptococcus mutans provide an important background for studies of the relationship between the historical spread of dental caries and anthropological factors.

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          Most cited references23

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          Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen.

          Streptococcus mutans is the leading cause of dental caries (tooth decay) worldwide and is considered to be the most cariogenic of all of the oral streptococci. The genome of S. mutans UA159, a serotype c strain, has been completely sequenced and is composed of 2,030,936 base pairs. It contains 1,963 ORFs, 63% of which have been assigned putative functions. The genome analysis provides further insight into how S. mutans has adapted to surviving the oral environment through resource acquisition, defense against host factors, and use of gene products that maintain its niche against microbial competitors. S. mutans metabolizes a wide variety of carbohydrates via nonoxidative pathways, and all of these pathways have been identified, along with the associated transport systems whose genes account for almost 15% of the genome. Virulence genes associated with extracellular adherent glucan production, adhesins, acid tolerance, proteases, and putative hemolysins have been identified. Strain UA159 is naturally competent and contains all of the genes essential for competence and quorum sensing. Mobile genetic elements in the form of IS elements and transposons are prominent in the genome and include a previously uncharacterized conjugative transposon and a composite transposon containing genes for the synthesis of antibiotics of the gramicidin/bacitracin family; however, no bacteriophage genomes are present.
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            Sugars and dental caries.

            A dynamic relation exists between sugars and oral health. Diet affects the integrity of the teeth; quantity, pH, and composition of the saliva; and plaque pH. Sugars and other fermentable carbohydrates, after being hydrolyzed by salivary amylase, provide substrate for the actions of oral bacteria, which in turn lower plaque and salivary pH. The resultant action is the beginning of tooth demineralization. Consumed sugars are naturally occurring or are added. Many factors in addition to sugars affect the caries process, including the form of food or fluid, the duration of exposure, nutrient composition, sequence of eating, salivary flow, presence of buffers, and oral hygiene. Studies have confirmed the direct relation between intake of dietary sugars and dental caries across the life span. Since the introduction of fluoride, the incidence of caries worldwide has decreased, despite increases in sugars consumption. Other dietary factors (eg, the presence of buffers in dairy products; the use of sugarless chewing gum, particularly gum containing xylitol; and the consumption of sugars as part of meals rather than between meals) may reduce the risk of caries. The primary public health measures for reducing caries risk, from a nutrition perspective, are the consumption of a balanced diet and adherence to dietary guidelines and the dietary reference intakes; from a dental perspective, the primary public health measures are the use of topical fluorides and consumption of fluoridated water.
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              Horizontal gene transfer accelerates genome innovation and evolution.

              Horizontal gene transfer (HGT) spreads genetic diversity by moving genes across species boundaries. By rapidly introducing newly evolved genes into existing genomes, HGT circumvents the slow step of ab initio gene creation and accelerates genome innovation. However, HGT can only affect organisms that readily exchange genes (exchange communities). In order to define exchange communities and understand the internal and external environmental factors that regulate HGT, we analyzed approximately 20,000 genes contained in eight free-living prokaryotic genomes. These analyses indicate that HGT occurs among organisms that share similar factors. The most significant are genome size, genome G/C composition, carbon utilization, and oxygen tolerance.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                18 July 2012
                2012
                : 2
                : 518
                Affiliations
                [1 ]simpleDepartment of Pediatric Dentistry, Nagasaki University Graduate School of Biomedical Sciences , 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
                [2 ]simpleDepartment of Oral and Molecular Microbiology, Osaka University Graduate School of Dentistry , 1–8 Yamadaoka, Suita, Osaka 565-0871, Japan
                Author notes
                Article
                srep00518
                10.1038/srep00518
                3399136
                22816041
                9e85fd24-c250-48f2-905c-f8de41077a8c
                Copyright © 2012, Macmillan Publishers Limited. All rights reserved

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareALike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

                History
                : 04 May 2012
                : 03 July 2012
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