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      A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum

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          Abstract

          The Spirochaetes species cause many important diseases including syphilis and Lyme disease. Except for their containing a distinctive endoflagella, no other molecular or biochemical characteristics are presently known that are specific for either all Spirochaetes or its different families. We report detailed comparative and phylogenomic analyses of protein sequences from Spirochaetes genomes to understand their evolutionary relationships and to identify molecular signatures for this group. These studies have identified 38 conserved signature indels (CSIs) that are specific for either all members of the phylum Spirochaetes or its different main clades. Of these CSIs, a 3 aa insert in the FlgC protein is uniquely shared by all sequenced Spirochaetes providing a molecular marker for this phylum. Seven, six, and five CSIs in different proteins are specific for members of the families Spirochaetaceae, Brachyspiraceae, and Leptospiraceae, respectively. Of the 19 other identified CSIs, 3 are uniquely shared by members of the genera Sphaerochaeta, Spirochaeta, and Treponema, whereas 16 others are specific for the genus Borrelia. A monophyletic grouping of the genera Sphaerochaeta, Spirochaeta, and Treponema distinct from the genus Borrelia is also strongly supported by phylogenetic trees based upon concatenated sequences of 22 conserved proteins. The molecular markers described here provide novel and more definitive means for identification and demarcation of different main groups of Spirochaetes. To accommodate the extensive genetic diversity of the Spirochaetes as revealed by different CSIs and phylogenetic analyses, it is proposed that the four families of this phylum should be elevated to the order level taxonomic ranks (viz. Spirochaetales, Brevinematales ord. nov., Brachyspiriales ord. nov., and Leptospiriales ord. nov.). It is further proposed that the genera Borrelia and Cristispira be transferred to a new family Borreliaceae fam. nov. within the order Spirochaetales.

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          Most cited references 69

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          Leptospira and leptospirosis.

          Leptospirosis is the most wide spread zoonosis worldwide; it is present in all continents except Antarctica and evidence for the carriage of Leptospira has been found in virtually all mammalian species examined. Humans most commonly become infected through occupational, recreational, or domestic contact with the urine of carrier animals, either directly or via contaminated water or soil. Leptospires are thin, helical bacteria classified into at least 12 pathogenic and 4 saprophytic species, with more than 250 pathogenic serovars. Immunity following infection is generally, but not exclusively, mediated by antibody against leptospiral LPS and restricted to antigenically related serovars. Vaccines currently available consist of killed whole cell bacterins which are used widely in animals, but less so in humans. Current work with recombinant protein antigens shows promise for the development of vaccines based on defined protective antigens. The cellular and molecular basis for virulence remains poorly understood, but comparative genomics of pathogenic and saprophytic species suggests that Leptospira expresses unique virulence determinants. However, the recent development of defined mutagenesis systems for Leptospira heralds the potential for gaining a much improved understanding of pathogenesis in leptospirosis. Copyright 2009 Elsevier B.V. All rights reserved.
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            Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi.

            The genome of the bacterium Borrelia burgdorferi B31, the aetiologic agent of Lyme disease, contains a linear chromosome of 910,725 base pairs and at least 17 linear and circular plasmids with a combined size of more than 533,000 base pairs. The chromosome contains 853 genes encoding a basic set of proteins for DNA replication, transcription, translation, solute transport and energy metabolism, but, like Mycoplasma genitalium, it contains no genes for cellular biosynthetic reactions. Because B. burgdorferi and M. genitalium are distantly related eubacteria, we suggest that their limited metabolic capacities reflect convergent evolution by gene loss from more metabolically competent progenitors. Of 430 genes on 11 plasmids, most have no known biological function; 39% of plasmid genes are paralogues that form 47 gene families. The biological significance of the multiple plasmid-encoded genes is not clear, although they may be involved in antigenic variation or immune evasion.
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              Prokaryotic evolution in light of gene transfer.

              Accumulating prokaryotic gene and genome sequences reveal that the exchange of genetic information through both homology-dependent recombination and horizontal (lateral) gene transfer (HGT) is far more important, in quantity and quality, than hitherto imagined. The traditional view, that prokaryotic evolution can be understood primarily in terms of clonal divergence and periodic selection, must be augmented to embrace gene exchange as a creative force, itself responsible for much of the pattern of similarities and differences we see between prokaryotic microbes. Rather than replacing periodic selection on genetic diversity, gene loss, and other chromosomal alterations as important players in adaptive evolution, gene exchange acts in concert with these processes to provide a rich explanatory paradigm-some of whose implications we explore here. In particular, we discuss (1) the role of recombination and HGT in giving phenotypic "coherence" to prokaryotic taxa at all levels of inclusiveness, (2) the implications of these processes for the reconstruction and meaning of "phylogeny," and (3) new views of prokaryotic adaptation and diversification based on gene acquisition and exchange.
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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                04 July 2013
                30 July 2013
                2013
                : 4
                Affiliations
                Department of Biochemistry and Biomedical Sciences, McMaster University Hamilton, ON, Canada
                Author notes

                Edited by: Hiromi Nishida, Toyama Prefectural University, Japan

                Reviewed by: Viktoria Shcherbakova, Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Russia; David L. Bernick, University of California, Santa Cruz, USA

                *Correspondence: Radhey S. Gupta, Department of Biochemistry and Biomedical Sciences, McMaster University, 1280 Main Street West, Hamilton, ON L8N 3Z5, Canada e-mail: gupta@ 123456mcmaster.ca

                This article was submitted to Frontiers in Evolutionary and Genomic Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2013.00217
                3726837
                23908650
                Copyright © 2013 Gupta, Mahmood and Adeolu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 8, Tables: 5, Equations: 0, References: 81, Pages: 18, Words: 10228
                Categories
                Microbiology
                Original Research Article

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