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Firmicutes-enriched IS1447 represents a group of IS3-family insertion sequences exhibiting unique + 1 transcriptional slippage

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      Abstract

      Background

      Bacterial insertion sequences (ISs) are ubiquitous mobile genetic elements that play important roles in genome plasticity, cell adaptability, and function evolution. ISs of various families and subgroups contain significantly diverse molecular features and functional mechanisms that are not fully understood.

      Results

      IS 1447 is a member of the widespread IS 3 family and was previously detected to have transposing activity in a typical thermophilic and cellulolytic microorganism Clostridium thermocellum. Phylogenetic analysis showed that IS 1447-like elements are widely distributed in Firmicutes and possess unique features in the IS 3 family. Therefore, IS 1447 may represent a novel subgroup of the IS 3 family. Unlike other well-known IS 3 subgroups performing programmed − 1 translational frameshifting for the expression of the transposase, IS 1447 exhibits transcriptional slippage in both the + 1 and − 1 directions, each with a frequency of ~ 16%, and only + 1 slippage results in full-length and functional transposase. The slippage-prone region of IS 1447 contains a run of nine A nucleotides following a stem-loop structure in mRNA, but mutagenesis analysis indicated that seven of them are sufficient for the observed slippage. Western blot analysis indicated that IS 1447 produces three types of transposases with alternative initiations. Furthermore, the IS 1447-subgroup elements are abundant in the genomes of several cellulolytic bacteria.

      Conclusion

      Our result indicated that IS 1447 represents a new Firmicutes-enriched subgroup of the IS 3 family. The characterization of the novel IS 3-family member will enrich our understanding of the transposition behavior of IS elements and may provide insight into developing IS-based mutagenesis tools for thermophiles.

      Electronic supplementary material

      The online version of this article (10.1186/s13068-018-1304-8) contains supplementary material, which is available to authorized users.

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      Most cited references 62

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        MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.

        Comparative analysis of molecular sequence data is essential for reconstructing the evolutionary histories of species and inferring the nature and extent of selective forces shaping the evolution of genes and species. Here, we announce the release of Molecular Evolutionary Genetics Analysis version 5 (MEGA5), which is a user-friendly software for mining online databases, building sequence alignments and phylogenetic trees, and using methods of evolutionary bioinformatics in basic biology, biomedicine, and evolution. The newest addition in MEGA5 is a collection of maximum likelihood (ML) analyses for inferring evolutionary trees, selecting best-fit substitution models (nucleotide or amino acid), inferring ancestral states and sequences (along with probabilities), and estimating evolutionary rates site-by-site. In computer simulation analyses, ML tree inference algorithms in MEGA5 compared favorably with other software packages in terms of computational efficiency and the accuracy of the estimates of phylogenetic trees, substitution parameters, and rate variation among sites. The MEGA user interface has now been enhanced to be activity driven to make it easier for the use of both beginners and experienced scientists. This version of MEGA is intended for the Windows platform, and it has been configured for effective use on Mac OS X and Linux desktops. It is available free of charge from http://www.megasoftware.net.
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          The neighbor-joining method: a new method for reconstructing phylogenetic trees.

           N Saitou,  M Nei (1987)
          A new method called the neighbor-joining method is proposed for reconstructing phylogenetic trees from evolutionary distance data. The principle of this method is to find pairs of operational taxonomic units (OTUs [= neighbors]) that minimize the total branch length at each stage of clustering of OTUs starting with a starlike tree. The branch lengths as well as the topology of a parsimonious tree can quickly be obtained by using this method. Using computer simulation, we studied the efficiency of this method in obtaining the correct unrooted tree in comparison with that of five other tree-making methods: the unweighted pair group method of analysis, Farris's method, Sattath and Tversky's method, Li's method, and Tateno et al.'s modified Farris method. The new, neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods.
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            Author and article information

            Affiliations
            [1 ]ISNI 0000000119573309, GRID grid.9227.e, CAS Key Laboratory of Biofuels, Shandong Provincial Key Laboratory of Energy Genetics, Qingdao Institute of Bioenergy and Bioprocess Technology, , Chinese Academy of Sciences, ; Qingdao, China
            [2 ]GRID grid.410752.5, Dalian National Laboratory for Clean Energy, ; Dalian, China
            [3 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, University of Chinese Academy of Sciences, Chinese Academy of Sciences, ; Beijing, China
            [4 ]ISNI 0000 0001 2297 8753, GRID grid.252546.2, Present Address: Department of Biosystems Engineering, , Auburn University, ; Auburn, AL 36849 USA
            Contributors
            liuyj@qibebt.ac.cn
            qikuan@qibebt.ac.cn
            zhangjie7008@outlook.com
            chenchao@qibebt.ac.cn
            cuiqiu@qibebt.ac.cn
            ORCID: http://orcid.org/0000-0002-0879-1316, fengyg@qibebt.ac.cn
            Journal
            Biotechnol Biofuels
            Biotechnol Biofuels
            Biotechnology for Biofuels
            BioMed Central (London )
            1754-6834
            1 November 2018
            1 November 2018
            2018
            : 11
            6211511
            1304
            10.1186/s13068-018-1304-8
            © The Author(s) 2018

            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.

            Funding
            Funded by: Strategic Priority Research Program of the Chinese Academy of Sciences
            Award ID: XDA 21060201
            Award Recipient :
            Funded by: National Key Technology Research and Development Program of China
            Award ID: 2015BAD15B05
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
            Award ID: 31570029
            Award ID: 31670735
            Award ID: 31661143023
            Award Recipient :
            Funded by: Key Technology Research and Development Program of Shandong
            Award ID: 2018GSF1160165
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/501100007129, Natural Science Foundation of Shandong Province;
            Award ID: ZR2016CB09
            Award Recipient :
            Funded by: the Major Program of Shandong Provincial Natural Science Foundation
            Award ID: ZR2018ZB0208
            Award Recipient :
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            © The Author(s) 2018

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