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      Bacteriophage and their potential roles in the human oral cavity

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          Abstract

          The human oral cavity provides the perfect portal of entry for viruses and bacteria in the environment to access new hosts. Hence, the oral cavity is one of the most densely populated habitats of the human body containing some 6 billion bacteria and potentially 35 times that many viruses. The role of these viral communities remains unclear; however, many are bacteriophage that may have active roles in shaping the ecology of oral bacterial communities. Other implications for the presence of such vast oral phage communities include accelerating the molecular diversity of their bacterial hosts as both host and phage mutate to gain evolutionary advantages. Additional roles include the acquisitions of new gene functions through lysogenic conversions that may provide selective advantages to host bacteria in response to antibiotics or other types of disturbances, and protection of the human host from invading pathogens by binding to and preventing pathogens from crossing oral mucosal barriers. Recent evidence suggests that phage may be more involved in periodontal diseases than were previously thought, as their compositions in the subgingival crevice in moderate to severe periodontitis are known to be significantly altered. However, it is unclear to what extent they contribute to dysbiosis or the transition of the microbial community into a state promoting oral disease. Bacteriophage communities are distinct in saliva compared to sub- and supragingival areas, suggesting that different oral biogeographic niches have unique phage ecology shaping their bacterial biota. In this review, we summarize what is known about phage communities in the oral cavity, the possible contributions of phage in shaping oral bacterial ecology, and the risks to public health oral phage may pose through their potential to spread antibiotic resistance gene functions to close contacts.

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          Most cited references85

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          Microbial ecology of dental plaque and its significance in health and disease.

          P.D. Marsh (1994)
          Dental plaque forms naturally on teeth and is of benefit to the host by helping to prevent colonization by exogenous species. The bacterial composition of plaque remains relatively stable despite regular exposure to minor environmental perturbations. This stability (microbial homeostasis) is due in part to a dynamic balance of both synergistic and antagonistic microbial interactions. However, homeostasis can break down, leading to shifts in the balance of the microflora, thereby predisposing sites to disease. For example, the frequent exposure of plaque to low pH leads to inhibition of acid-sensitive species and the selection of organisms with an aciduric physiology, such as mutans streptococci and lactobacilli. Similarly, plaque accumulation around the gingival margin leads to an inflammatory host response and an increased flow of gingival crevicular fluid. The subgingival microflora shifts from being mainly Gram-positive to being comprised of increased levels of obligately anaerobic, asaccharolytic Gram-negative organisms. It is proposed that disease can be prevented or treated not only by targeting the putative pathogens but also by interfering with the processes that drive the breakdown in homeostasis. Thus, the rate of acid production following sugar intake could be reduced by fluoride, alternative sweeteners, and low concentrations of antimicrobial agents, while oxygenating or redox agents could raise the Eh of periodontal pockets and prevent the growth and metabolism of obligately anaerobic species. These views have been incorporated into a modified hypothesis (the "ecological plaque hypothesis") to explain the relationship between the plaque microflora and the host in health and disease, and to identify new strategies for disease prevention.
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            Type IV pili and twitching motility.

            Twitching motility is a flagella-independent form of bacterial translocation over moist surfaces. It occurs by the extension, tethering, and then retraction of polar type IV pili, which operate in a manner similar to a grappling hook. Twitching motility is equivalent to social gliding motility in Myxococcus xanthus and is important in host colonization by a wide range of plant and animal pathogens, as well as in the formation of biofilms and fruiting bodies. The biogenesis and function of type IV pili is controlled by a large number of genes, almost 40 of which have been identified in Pseudomonas aeruginosa. A number of genes required for pili assembly are homologous to genes involved in type II protein secretion and competence for DNA uptake, suggesting that these systems share a common architecture. Twitching motility is also controlled by a range of signal transduction systems, including two-component sensor-regulators and a complex chemosensory system.
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              Bacteria-phage antagonistic coevolution in soil.

              Bacteria and their viruses (phages) undergo rapid coevolution in test tubes, but the relevance to natural environments is unclear. By using a "mark-recapture" approach, we showed rapid coevolution of bacteria and phages in a soil community. Unlike coevolution in vitro, which is characterized by increases in infectivity and resistance through time (arms race dynamics), coevolution in soil resulted in hosts more resistant to their contemporary than past and future parasites (fluctuating selection dynamics). Fluctuating selection dynamics, which can potentially continue indefinitely, can be explained by fitness costs constraining the evolution of high levels of resistance in soil. These results suggest that rapid coevolution between bacteria and phage is likely to play a key role in structuring natural microbial communities.
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                Author and article information

                Journal
                J Oral Microbiol
                J Oral Microbiol
                JOM
                Journal of Oral Microbiology
                Co-Action Publishing
                2000-2297
                09 April 2015
                2015
                : 7
                : 10.3402/jom.v7.27423
                Affiliations
                [1 ]Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, USA
                [2 ]School of Dentistry, University of California, Los Angeles, CA, USA
                [3 ]Department of Pathology, University of California, San Diego, CA, USA
                [4 ]Western University College of Dental Medicine, Pomona, CA, USA
                [5 ]Department of Medicine, University of California, San Diego, CA, USA
                Author notes
                [* ]Correspondence to: David T. Pride, Department of Pathology, University of California, San Diego, 9500 Gilman Drive, MC 0612, La Jolla, CA 92093-0612, USA, Email: dpride@ 123456ucsd.edu
                Article
                27423
                10.3402/jom.v7.27423
                4393417
                25861745
                9ea892b7-3dba-4cee-8807-a29dac55bcae
                © 2015 Anna Edlund et al.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License, permitting all non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 January 2015
                : 11 March 2015
                : 13 March 2015
                Categories
                Review Article

                Microbiology & Virology
                bacteriophage,virus,microbiome,virome,metagenome,oral microbiome
                Microbiology & Virology
                bacteriophage, virus, microbiome, virome, metagenome, oral microbiome

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