Primordial origin and diversification of plasmids in Lyme disease agent bacteria

Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorfer...

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Veröffentlicht in:BMC genomics Jg. 19; H. 1; S. 218 - 24
Hauptverfasser: Casjens, Sherwood R., Di, Lia, Akther, Saymon, Mongodin, Emmanuel F., Luft, Benjamin J., Schutzer, Steven E., Fraser, Claire M., Qiu, Wei-Gang
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London BioMed Central 27.03.2018
BMC
Schlagworte:
Animal Genetics and Genomics
Biomedical and Life Sciences
Borrelia
Borrelia burgdorferi - classification
Borrelia burgdorferi - genetics
Borrelia burgdorferi - physiology
Borreliella
Burgdorferi
Chromosomes, Bacterial
Circular plasmid
Comparative and evolutionary genomics
DNA, Bacterial
Genome, Bacterial
Genomics - methods
High-Throughput Nucleotide Sequencing - methods
Humans
Life Sciences
Linear plasmid
Lyme disease
Lyme Disease - microbiology
Microarrays
Microbial Genetics and Genomics
Phylogeny
Plant Genetics and Genomics
Plasmids - genetics
Proteomics
Research Article
Sequence Analysis, DNA
Species Specificity
Lyme disease
Circular plasmid
Plasmid evolution
Linear plasmid
Borrelia
Borreliella
Burgdorferi
ISSN:1471-2164, 1471-2164
Online-Zugang:Volltext
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Abstract Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species. Results We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii , B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non- B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi . These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types. Conclusions The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.
AbstractList Abstract Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species. Results We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii, B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non-B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi. These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types. Conclusions The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.
Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species. Results We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii , B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non- B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi . These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types. Conclusions The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.
With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species. We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii, B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non-B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi. These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types. The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.
With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species.BACKGROUNDWith approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species.We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii, B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non-B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi. These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types.RESULTSWe sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii, B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non-B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi. These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types.The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.CONCLUSIONSThe primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.
ArticleNumber 218
Author Luft, Benjamin J.
Schutzer, Steven E.
Fraser, Claire M.
Mongodin, Emmanuel F.
Casjens, Sherwood R.
Di, Lia
Akther, Saymon
Qiu, Wei-Gang
Author_xml – sequence: 1
  givenname: Sherwood R.
  surname: Casjens
  fullname: Casjens, Sherwood R.
  email: sherwood.casjens@path.utah.edu
  organization: Division of Microbiology and Immunology, Pathology Department and Biology Department, University of Utah School of Medicine, Biology Department, University of Utah, Pathology Department, University of Utah School of Medicine
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  givenname: Lia
  surname: Di
  fullname: Di, Lia
  organization: Department of Biological Sciences and Center for Translational and Basic Research, Hunter College of the City University of New York
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  givenname: Saymon
  surname: Akther
  fullname: Akther, Saymon
  organization: Department of Biology, The Graduate Center, City University of New York
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  givenname: Emmanuel F.
  surname: Mongodin
  fullname: Mongodin, Emmanuel F.
  organization: Institute for Genome Sciences, University of Maryland School of Medicine
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  givenname: Benjamin J.
  surname: Luft
  fullname: Luft, Benjamin J.
  organization: Department of Medicine, Health Science Center, Stony Brook University
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  surname: Schutzer
  fullname: Schutzer, Steven E.
  organization: Department of Medicine, New Jersey Medical School, Rutgers, The State University of New Jersey
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  givenname: Claire M.
  surname: Fraser
  fullname: Fraser, Claire M.
  organization: Institute for Genome Sciences, University of Maryland School of Medicine
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  givenname: Wei-Gang
  orcidid: 0000-0003-4585-1872
  surname: Qiu
  fullname: Qiu, Wei-Gang
  email: weigang@genectr.hunter.cuny.edu
  organization: Department of Biology, The Graduate Center, City University of New York, Department of Biological Sciences and Center for Translational and Basic Research, Hunter College of the City University of New York, Department of Physiology and Biophysics & Institute for Computational Biomedicine, Weil Cornell Medical College
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29580205$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Lyme disease
Circular plasmid
Plasmid evolution
Linear plasmid
Borrelia
Borreliella
Burgdorferi
Language English
License 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.
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Snippet Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most...
With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex...
Abstract Background With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the...
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StartPage 218
SubjectTerms Animal Genetics and Genomics
Biomedical and Life Sciences
Borrelia
Borrelia burgdorferi - classification
Borrelia burgdorferi - genetics
Borrelia burgdorferi - physiology
Borreliella
Burgdorferi
Chromosomes, Bacterial
Circular plasmid
Comparative and evolutionary genomics
DNA, Bacterial
Genome, Bacterial
Genomics - methods
High-Throughput Nucleotide Sequencing - methods
Humans
Life Sciences
Linear plasmid
Lyme disease
Lyme Disease - microbiology
Microarrays
Microbial Genetics and Genomics
Phylogeny
Plant Genetics and Genomics
Plasmids - genetics
Proteomics
Research Article
Sequence Analysis, DNA
Species Specificity
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Title Primordial origin and diversification of plasmids in Lyme disease agent bacteria
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