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      Comparative genomic analysis of Clostridium difficile ribotype 027 strains including the newly sequenced strain NCKUH-21 isolated from a patient in Taiwan

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          Abstract

          Background

          Clostridium difficile is a Gram-positive anaerobe and the leading cause of antibiotic-associated diarrhea worldwide. The emergence of ribotype 027 (RT027) strains is associated with increased incidence of infection and mortality. To further understand the relationship between C. difficile NCKUH-21, a RT027 strain isolated from a patient in Taiwan, and other RT027 strains, we performed whole-genome shotgun sequencing on NCKUH-21 and comparative genomic analyses.

          Results

          The genome size, G+C content, and gene number for the NCKUH-21 strain were determined to be similar to those for other C. difficile strains. The core genome phylogeny indicated that the five RT027 strains R20291, CD196, NCKUH-21, BI1, and 2007855 formed a clade. A pathogenicity locus, tcdR- tcdB- tcdE- orf- tcdA- tcdC, was conserved in the genome. A genomic region highly similar to the Clostridium phage \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\upvarphi$$\end{document} CD38-2 was present in the NCKUH-21 strain but absent in the other RT027 strains and designated as the prophage \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\upvarphi$$\end{document} NCKUH-21. The prophage \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\upvarphi$$\end{document} NCKUH-21 genes were significantly higher in G+C content than the other genes in the NCKUH-21 genome, indicating that the prophage does not match the base composition of the host genome.

          Conclusions

          This is the first whole-genome analysis of a RT027 C. difficile strain isolated from Taiwan. Due to the high identity with \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\upvarphi$$\end{document} CD38-2, the prophage identified in the NCKUH-21 genome has the potential to regulate toxin production. These results provide important information for understanding the pathogenicity of RT027 C. difficile in Taiwan.

          Electronic supplementary material

          The online version of this article (10.1186/s13099-017-0219-4) contains supplementary material, which is available to authorized users.

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          Most cited references15

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          Amelioration of bacterial genomes: rates of change and exchange.

          Although bacterial species display wide variation in their overall GC contents, the genes within a particular species' genome are relatively similar in base composition. As a result, sequences that are novel to a bacterial genome-i.e., DNA introduced through recent horizontal transfer-often bear unusual sequence characteristics and can be distinguished from ancestral DNA. At the time of introgression, horizontally transferred genes reflect the base composition of the donor genome; but, over time, these sequences will ameliorate to reflect the DNA composition of the new genome because the introgressed genes are subject to the same mutational processes affecting all genes in the recipient genome. This process of amelioration is evident in a large group of genes involved in host-cell invasion by enteric bacteria and can be modeled to predict the amount of time required after transfer for foreign DNA to resemble native DNA. Furthermore, models of amelioration can be used to estimate the time of introgression of foreign genes in a chromosome. Applying this approach to a 1.43-megabase continuous sequence, we have calculated that the entire Escherichia coli chromosome contains more than 600 kb of horizontally transferred, protein-coding DNA. Estimates of amelioration times indicate that this DNA has accumulated at a rate of 31 kb per million years, which is on the order of the amount of variant DNA introduced by point mutations. This rate predicts that the E. coli and Salmonella enterica lineages have each gained and lost more than 3 megabases of novel DNA since their divergence.
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            Base composition bias might result from competition for metabolic resources.

            The GC content of bacterial genomes varies from 25 to 75%, but the reason for this variation is unclear. Here, we show that genomes of bacteria that rely on their host for survival (obligatory pathogens or symbionts) tend to be AT rich. Furthermore, we have analysed bacterial phages, plasmids and insertion sequences, which might also be regarded as 'intracellular pathogens', and show that they too are significantly richer in AT than their hosts. We suggest that the higher energy cost and limited availability of G and C over A and T/U could be a basis for the understanding of these differences.
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              Clinical recognition and diagnosis of Clostridium difficile infection.

              Prompt and precise diagnosis is an important aspect of effective management of Clostridium difficile infection (CDI). CDI causes 15%-25% of all cases of antibiotic-associated diarrhea, the severity of which ranges from mild diarrhea to fulminant pseudomembranous colitis. Several factors, especially advanced age and hospitalization, should be considered in the diagnosis of CDI. In particular, nosocomial diarrhea arising >72 hours after admission among patients receiving antibiotics is highly likely to have resulted from CDI. Testing of stool for the presence of C. difficile toxin confirms the diagnosis of CDI. However, performance of an enzyme immunoassay is the usual method by which CDI is confirmed, but this test appears to be relatively insensitive, compared with the cell cytotoxicity assay and stool culture for toxigenic C. difficile on selective medium. Endoscopy and computed tomography are less sensitive than stool toxin assays but may be useful when immediate results are important or other confounding conditions rank high in the differential diagnosis. Often overlooked aspects of this diagnosis are high white blood cell counts (which are sometimes in the leukemoid range) and hypoalbuminemia.
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                Author and article information

                Contributors
                haruo@sfc.keio.ac.jp
                mt@sfc.keio.ac.jp
                pjtsai219@gmail.com
                winston3415@gmail.com
                yuebin16@yahoo.com.tw
                +886-6-235-3535 , ihsiuhuang@mail.ncku.edu.tw
                +886-6-235-3535 , jc923@mail.ncku.edu.tw
                Journal
                Gut Pathog
                Gut Pathog
                Gut Pathogens
                BioMed Central (London )
                1757-4749
                29 November 2017
                29 November 2017
                2017
                : 9
                : 70
                Affiliations
                [1 ]ISNI 0000 0004 1936 9959, GRID grid.26091.3c, Institute for Advanced Biosciences, , Keio University, ; Tsuruoka, Yamagata Japan
                [2 ]ISNI 0000 0004 1936 9959, GRID grid.26091.3c, Faculty of Environment and Information Studies, , Keio University, ; Fujisawa, Kanagawa Japan
                [3 ]ISNI 0000 0004 0532 3255, GRID grid.64523.36, Department of Medical Laboratory Science and Biotechnology, , National Cheng Kung University, ; Tainan, Taiwan
                [4 ]ISNI 0000 0004 0532 3255, GRID grid.64523.36, Department of Medicine, College of Medicine, , National Cheng Kung University , ; Tainan, Taiwan
                [5 ]GRID grid.454740.6, Department of Internal Medicine, Tainan Hospital, , Ministry of Health & Welfare, ; Tainan, Taiwan
                [6 ]ISNI 0000 0004 0639 0054, GRID grid.412040.3, Department of Internal Medicine, , National Cheng Kung University Hospital, ; Tainan, Taiwan
                [7 ]ISNI 0000 0004 0532 3255, GRID grid.64523.36, Department of Microbiology and Immunology, College of Medicine, , National Cheng Kung University, ; 1 University Road, Tainan, 70101 Taiwan
                Author information
                http://orcid.org/0000-0002-5433-5178
                Article
                219
                10.1186/s13099-017-0219-4
                5708112
                2d6534c1-719d-4b6f-8c4f-f8e91cc0a517
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 October 2017
                : 21 November 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001697, Keio University;
                Funded by: Yamagata Prefecture and Tsuruoka City, Japan
                Funded by: FundRef http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: MOST103-2320-B-006-028-MY2
                Award ID: MOST106-2633-B-006-002-
                Award Recipient :
                Categories
                Genome Report
                Custom metadata
                © The Author(s) 2017

                Gastroenterology & Hepatology
                clostridium difficile,ribotype 027 strain nckuh-21,genome,phylogeny,prophage,horizontal transfer

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