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      Comparative genomic analysis of six new-found integrative conjugative elements (ICEs) in Vibrio alginolyticus

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          Abstract

          Background

          Vibrio alginolyticus is ubiquitous in marine and estuarine environments. In 2012–2013, SXT/R391-like integrative conjugative elements (ICEs) in environmental V. alginolyticus strains were discovered and found to occur in 8.9 % of 192  V. alginolyticus strains, which suggests that V. alginolyticus may be a natural pool possessing resourceful ICEs. However, complete ICE sequences originating from this bacterium have not been reported, which represents a significant barrier to characterizing the ICEs of this bacterium and exploring their relationships with other ICEs. In the present study, we acquired six ICE sequences from five V. alginolyticus strains and performed a comparative analysis of these ICE genomes.

          Results

          A sequence analysis showed that there were only 14 variable bases dispersed between ICE ValE0601 and ICE ValHN492. ICE ValE0601 and ICE ValHN492 were treated as the same ICE. ICE ValA056-1, ICE ValE0601 and ICE ValHN492 integrate into the 5′ end of the host’s prfC gene, and their Int and Xis share at least 97 % identity with their counterparts from SXT. ICE ValE0601 or ICE ValHN492 contain 50 of 52 conserved core genes in the SXT/R391 ICEs (not s025 or s026) . ICE ValA056-2, ICE ValHN396 and ICE ValHN437 have a different tRNA-ser integration site and a distinct int/xis module; however, the remaining backbone genes are highly similar to their counterparts in SXT/R391 ICEs. DNA sequences inserted into hotspot and variable regions of the ICEs are of various sizes. The variable genes of six ICEs encode a large array of functions to bestow various adaptive abilities upon their hosts, and only ICE ValA056-1 contains drug-resistant genes. Many variable genes have orthologous and functionally related genes to those found in SXT/R391 ICEs, such as genes coding for a toxin-antitoxin system, a restriction-modification system, helicases and endonucleases. Six ICEs also contain a large number of unique genes or gene clusters that were not found in other ICEs. Six ICEs harbor more abundant transposase genes compared with other parts of their host genomes. A phylogenetic analysis indicated that transposase genes in these ICEs are highly diverse.

          Conclusions

          ICE ValA056-1, ICE ValE0601 and ICE ValHN492 are typical members of the SXT/R391 family. ICE ValA056-2, ICE ValHN396 and ICE ValHN437 form a new atypical group belonging to the SXT/R391 family. In addition to the many genes found to be present in other ICEs, six ICEs contain a large number of unique genes or gene clusters that were not found in other ICEs. ICEs may serve as a carrier for transposable genetic elements (TEs) and largely facilitate the dissemination of TEs.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12866-016-0692-9) contains supplementary material, which is available to authorized users.

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          Most cited references49

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          Making sense of it all: bacterial chemotaxis.

          Bacteria must be able to respond to a changing environment, and one way to respond is to move. The transduction of sensory signals alters the concentration of small phosphorylated response regulators that bind to the rotary flagellar motor and cause switching. This simple pathway has provided a paradigm for sensory systems in general. However, the increasing number of sequenced bacterial genomes shows that although the central sensory mechanism seems to be common to all bacteria, there is added complexity in a wide range of species.
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            Which transposable elements are active in the human genome?

            Although a large proportion (44%) of the human genome is occupied by transposons and transposon-like repetitive elements, only a small proportion (<0.05%) of these elements remain active today. Recent evidence indicates that approximately 35-40 subfamilies of Alu, L1 and SVA elements (and possibly HERV-K elements) remain actively mobile in the human genome. These active transposons are of great interest because they continue to produce genetic diversity in human populations and also cause human diseases by integrating into genes. In this review, we examine these active human transposons and explore mechanistic factors that influence their mobilization.
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              Insertion sequences.

              Insertion sequences (ISs) constitute an important component of most bacterial genomes. Over 500 individual ISs have been described in the literature to date, and many more are being discovered in the ongoing prokaryotic and eukaryotic genome-sequencing projects. The last 10 years have also seen some striking advances in our understanding of the transposition process itself. Not least of these has been the development of various in vitro transposition systems for both prokaryotic and eukaryotic elements and, for several of these, a detailed understanding of the transposition process at the chemical level. This review presents a general overview of the organization and function of insertion sequences of eubacterial, archaebacterial, and eukaryotic origins with particular emphasis on bacterial elements and on different aspects of the transposition mechanism. It also attempts to provide a framework for classification of these elements by assigning them to various families or groups. A total of 443 members of the collection have been grouped in 17 families based on combinations of the following criteria: (i) similarities in genetic organization (arrangement of open reading frames); (ii) marked identities or similarities in the enzymes which mediate the transposition reactions, the recombinases/transposases (Tpases); (iii) similar features of their ends (terminal IRs); and (iv) fate of the nucleotide sequence of their target sites (generation of a direct target duplication of determined length). A brief description of the mechanism(s) involved in the mobility of individual ISs in each family and of the structure-function relationships of the individual Tpases is included where available.
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                Author and article information

                Contributors
                hucq@scsio.ac.cn
                Journal
                BMC Microbiol
                BMC Microbiol
                BMC Microbiology
                BioMed Central (London )
                1471-2180
                4 May 2016
                4 May 2016
                2016
                : 16
                : 79
                Affiliations
                [ ]Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301 China
                [ ]Guangdong Key Laboratory of Applied Marine Biology, Chinese Academy of Sciences, Guangzhou, 510301 China
                [ ]South China Sea Bio-Resource Exploitation and Utilization Collaborative Innovation Center, Guangzhou, 510275 China
                [ ]University of Chinese Academy of Sciences, Beijing, 100049 China
                Article
                692
                10.1186/s12866-016-0692-9
                4857294
                27145747
                f4b09731-3f62-4677-907e-03baa92ca95d
                © Luo et al. 2016

                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
                : 28 June 2015
                : 14 April 2016
                Funding
                Funded by: Natural Science Foundation of China
                Award ID: 31370149
                Award Recipient :
                Funded by: Comprehensive Strategic Cooperation Project of Guangdong Province and Chinese Academy of Sciences
                Award ID: 2012B091100269
                Award Recipient :
                Funded by: Knowledge Innovation Program of CAS
                Award ID: KSCX2-EW-G-12B
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Microbiology & Virology
                vibrio alginolyticus,integrative conjugative elements (ices),comparative genomics,transposable genetic elements (tes)

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