Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity

Abstract Background Tick-borne relapsing fever (TBRF) is a globally prevalent, yet under-studied vector-borne disease transmitted by soft and hard bodied ticks. While soft TBRF (sTBRF) spirochetes have been described for over a century, our understanding of the molecular mechanisms facilitating vect...

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Main Authors: Alexander R. Kneubehl, Aparna Krishnavajhala, Sebastián Muñoz Leal, Adam J. Replogle, Luke C. Kingry, Sergio E. Bermúdez, Marcelo B. Labruna, Job E. Lopez
Format: Article
Language:English
Published: BMC 2022-05-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-022-08523-7
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author Alexander R. Kneubehl
Aparna Krishnavajhala
Sebastián Muñoz Leal
Adam J. Replogle
Luke C. Kingry
Sergio E. Bermúdez
Marcelo B. Labruna
Job E. Lopez
author_facet Alexander R. Kneubehl
Aparna Krishnavajhala
Sebastián Muñoz Leal
Adam J. Replogle
Luke C. Kingry
Sergio E. Bermúdez
Marcelo B. Labruna
Job E. Lopez
author_sort Alexander R. Kneubehl
collection DOAJ
description Abstract Background Tick-borne relapsing fever (TBRF) is a globally prevalent, yet under-studied vector-borne disease transmitted by soft and hard bodied ticks. While soft TBRF (sTBRF) spirochetes have been described for over a century, our understanding of the molecular mechanisms facilitating vector and host adaptation is poorly understood. This is due to the complexity of their small (~ 1.5 Mb) but fragmented genomes that typically consist of a linear chromosome and both linear and circular plasmids. A majority of sTBRF spirochete genomes’ plasmid sequences are either missing or are deposited as unassembled sequences. Consequently, our goal was to generate complete, plasmid-resolved genomes for a comparative analysis of sTBRF species of the Western Hemisphere. Results Utilizing a Borrelia specific pipeline, genomes of sTBRF spirochetes from the Western Hemisphere were sequenced and assembled using a combination of short- and long-read sequencing technologies. Included in the analysis were the two recently isolated species from Central and South America, Borrelia puertoricensis n. sp. and Borrelia venezuelensis, respectively. Plasmid analyses identified diverse sequences that clustered plasmids into 30 families; however, only three families were conserved and syntenic across all species. We also compared two species, B. venezuelensis and Borrelia turicatae, which were isolated ~ 6,800 km apart and from different tick vector species but were previously reported to be genetically similar. Conclusions To truly understand the biological differences observed between species of TBRF spirochetes, complete chromosome and plasmid sequences are needed. This comparative genomic analysis highlights high chromosomal synteny across the species yet diverse plasmid composition. This was particularly true for B. turicatae and B. venezuelensis, which had high average nucleotide identity yet extensive plasmid diversity. These findings are foundational for future endeavors to evaluate the role of plasmids in vector and host adaptation.
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spelling doaj.art-66556ae6ca074a349a4a164bc1f0bb162022-12-22T03:22:26ZengBMCBMC Genomics1471-21642022-05-0123112210.1186/s12864-022-08523-7Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversityAlexander R. Kneubehl0Aparna Krishnavajhala1Sebastián Muñoz Leal2Adam J. Replogle3Luke C. Kingry4Sergio E. Bermúdez5Marcelo B. Labruna6Job E. Lopez7Department of Pediatrics, Baylor College of MedicineDepartment of Pediatrics, Baylor College of MedicineDepartamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de ConcepciónDivision of Vector-Borne Diseases, Centers for Disease Control and PreventionDivision of Vector-Borne Diseases, Centers for Disease Control and PreventionMedical Entomology Department, Gorgas Memorial Institute for Health ResearchDepartamento de Medicina Veterinária Preventiva E Saúde Animal, Faculdade de Medicina Veterinária E Zootecnia, Universidade de São PauloDepartment of Pediatrics, Baylor College of MedicineAbstract Background Tick-borne relapsing fever (TBRF) is a globally prevalent, yet under-studied vector-borne disease transmitted by soft and hard bodied ticks. While soft TBRF (sTBRF) spirochetes have been described for over a century, our understanding of the molecular mechanisms facilitating vector and host adaptation is poorly understood. This is due to the complexity of their small (~ 1.5 Mb) but fragmented genomes that typically consist of a linear chromosome and both linear and circular plasmids. A majority of sTBRF spirochete genomes’ plasmid sequences are either missing or are deposited as unassembled sequences. Consequently, our goal was to generate complete, plasmid-resolved genomes for a comparative analysis of sTBRF species of the Western Hemisphere. Results Utilizing a Borrelia specific pipeline, genomes of sTBRF spirochetes from the Western Hemisphere were sequenced and assembled using a combination of short- and long-read sequencing technologies. Included in the analysis were the two recently isolated species from Central and South America, Borrelia puertoricensis n. sp. and Borrelia venezuelensis, respectively. Plasmid analyses identified diverse sequences that clustered plasmids into 30 families; however, only three families were conserved and syntenic across all species. We also compared two species, B. venezuelensis and Borrelia turicatae, which were isolated ~ 6,800 km apart and from different tick vector species but were previously reported to be genetically similar. Conclusions To truly understand the biological differences observed between species of TBRF spirochetes, complete chromosome and plasmid sequences are needed. This comparative genomic analysis highlights high chromosomal synteny across the species yet diverse plasmid composition. This was particularly true for B. turicatae and B. venezuelensis, which had high average nucleotide identity yet extensive plasmid diversity. These findings are foundational for future endeavors to evaluate the role of plasmids in vector and host adaptation.https://doi.org/10.1186/s12864-022-08523-7Relapsing feverBorreliaComparative genomicsPlasmidsMicrobial genomicsLong-read sequencing
spellingShingle Alexander R. Kneubehl
Aparna Krishnavajhala
Sebastián Muñoz Leal
Adam J. Replogle
Luke C. Kingry
Sergio E. Bermúdez
Marcelo B. Labruna
Job E. Lopez
Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
BMC Genomics
Relapsing fever
Borrelia
Comparative genomics
Plasmids
Microbial genomics
Long-read sequencing
title Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
title_full Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
title_fullStr Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
title_full_unstemmed Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
title_short Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity
title_sort comparative genomics of the western hemisphere soft tick borne relapsing fever borreliae highlights extensive plasmid diversity
topic Relapsing fever
Borrelia
Comparative genomics
Plasmids
Microbial genomics
Long-read sequencing
url https://doi.org/10.1186/s12864-022-08523-7
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