Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity

Amy Fleshman, Kristin Mullins, Jason Sahl, Crystal Hepp, Nathan C Nieto, Kristin Wiggins, Heidie Hornstra, Daryl Kelly, Teik Chye Chan, Rattanaphone Phetsouvanh, Sabine Dittrich, Phonepasith Panyanivong, Daniel Paris, Paul Newton, Allen Richards, Talima R Pearson

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Orientia tsutsugamushi, formerly Rickettsia tsutsugamushi, is an obligate intracellular pathogen that causes scrub typhus, an underdiagnosed acute febrile disease with high morbidity. Scrub typhus is transmitted by the larval stage (chigger) of Leptotrombidium mites and is irregularly distributed across endemic regions of Asia, Australia and islands of the western Pacific Ocean. Previous work to understand population genetics in O. tsutsugamushi has been based on sub-genomic sampling methods and whole-genome characterization of two genomes. In this study, we compared 40 genomes from geographically dispersed areas and confirmed patterns of extensive homologous recombination likely driven by transposons, conjugative elements and repetitive sequences. High rates of lateral gene transfer (LGT) among O. tsutsugamushi genomes appear to have effectively eliminated a detectable clonal frame, but not our ability to infer evolutionary relationships and phylogeographical clustering. Pan-genomic comparisons using 31 082 high-quality bacterial genomes from 253 species suggests that genomic duplication in O. tsutsugamushi is almost unparalleled. Unlike other highly recombinant species where the uptake of exogenous DNA largely drives genomic diversity, the pan-genome of O. tsutsugamushi is driven by duplication and divergence. Extensive gene innovation by duplication is most commonly attributed to plants and animals and, in contrast with LGT, is thought to be only a minor evolutionary mechanism for bacteria. The near unprecedented evolutionary characteristics of O. tsutsugamushi, coupled with extensive intra-specific LGT, expand our present understanding of rapid bacterial evolutionary adaptive mechanisms.

Original languageEnglish (US)
JournalMicrobial genomics
Volume4
Issue number9
DOIs
StatePublished - Sep 1 2018

Fingerprint

Orientia tsutsugamushi
Horizontal Gene Transfer
Genome
Trombiculidae
Scrub Typhus
Pacific Ocean
Bacterial Genomes
Western Australia
Gene Duplication
Nucleic Acid Repetitive Sequences
Mites
Homologous Recombination
Population Genetics
Acute Disease
Islands
Cluster Analysis
Fever
Morbidity
Bacteria
DNA

Keywords

  • adaptive evolution
  • gene divergence
  • genome adaptation
  • lateral gene transfer
  • pan-genome
  • scrub typhus

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity. / Fleshman, Amy; Mullins, Kristin; Sahl, Jason; Hepp, Crystal; Nieto, Nathan C; Wiggins, Kristin; Hornstra, Heidie; Kelly, Daryl; Chan, Teik Chye; Phetsouvanh, Rattanaphone; Dittrich, Sabine; Panyanivong, Phonepasith; Paris, Daniel; Newton, Paul; Richards, Allen; Pearson, Talima R.

In: Microbial genomics, Vol. 4, No. 9, 01.09.2018.

Research output: Contribution to journalArticle

Fleshman, A, Mullins, K, Sahl, J, Hepp, C, Nieto, NC, Wiggins, K, Hornstra, H, Kelly, D, Chan, TC, Phetsouvanh, R, Dittrich, S, Panyanivong, P, Paris, D, Newton, P, Richards, A & Pearson, TR 2018, 'Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity', Microbial genomics, vol. 4, no. 9. https://doi.org/10.1099/mgen.0.000199
Fleshman, Amy ; Mullins, Kristin ; Sahl, Jason ; Hepp, Crystal ; Nieto, Nathan C ; Wiggins, Kristin ; Hornstra, Heidie ; Kelly, Daryl ; Chan, Teik Chye ; Phetsouvanh, Rattanaphone ; Dittrich, Sabine ; Panyanivong, Phonepasith ; Paris, Daniel ; Newton, Paul ; Richards, Allen ; Pearson, Talima R. / Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity. In: Microbial genomics. 2018 ; Vol. 4, No. 9.
@article{47726e9601e646eb8346899929f8e135,
title = "Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity",
abstract = "Orientia tsutsugamushi, formerly Rickettsia tsutsugamushi, is an obligate intracellular pathogen that causes scrub typhus, an underdiagnosed acute febrile disease with high morbidity. Scrub typhus is transmitted by the larval stage (chigger) of Leptotrombidium mites and is irregularly distributed across endemic regions of Asia, Australia and islands of the western Pacific Ocean. Previous work to understand population genetics in O. tsutsugamushi has been based on sub-genomic sampling methods and whole-genome characterization of two genomes. In this study, we compared 40 genomes from geographically dispersed areas and confirmed patterns of extensive homologous recombination likely driven by transposons, conjugative elements and repetitive sequences. High rates of lateral gene transfer (LGT) among O. tsutsugamushi genomes appear to have effectively eliminated a detectable clonal frame, but not our ability to infer evolutionary relationships and phylogeographical clustering. Pan-genomic comparisons using 31 082 high-quality bacterial genomes from 253 species suggests that genomic duplication in O. tsutsugamushi is almost unparalleled. Unlike other highly recombinant species where the uptake of exogenous DNA largely drives genomic diversity, the pan-genome of O. tsutsugamushi is driven by duplication and divergence. Extensive gene innovation by duplication is most commonly attributed to plants and animals and, in contrast with LGT, is thought to be only a minor evolutionary mechanism for bacteria. The near unprecedented evolutionary characteristics of O. tsutsugamushi, coupled with extensive intra-specific LGT, expand our present understanding of rapid bacterial evolutionary adaptive mechanisms.",
keywords = "adaptive evolution, gene divergence, genome adaptation, lateral gene transfer, pan-genome, scrub typhus",
author = "Amy Fleshman and Kristin Mullins and Jason Sahl and Crystal Hepp and Nieto, {Nathan C} and Kristin Wiggins and Heidie Hornstra and Daryl Kelly and Chan, {Teik Chye} and Rattanaphone Phetsouvanh and Sabine Dittrich and Phonepasith Panyanivong and Daniel Paris and Paul Newton and Allen Richards and Pearson, {Talima R}",
year = "2018",
month = "9",
day = "1",
doi = "10.1099/mgen.0.000199",
language = "English (US)",
volume = "4",
journal = "Microbial genomics",
issn = "2057-5858",
publisher = "Microbiology Society",
number = "9",

}

TY - JOUR

T1 - Comparative pan-genomic analyses of Orientia tsutsugamushi reveal an exceptional model of bacterial evolution driving genomic diversity

AU - Fleshman, Amy

AU - Mullins, Kristin

AU - Sahl, Jason

AU - Hepp, Crystal

AU - Nieto, Nathan C

AU - Wiggins, Kristin

AU - Hornstra, Heidie

AU - Kelly, Daryl

AU - Chan, Teik Chye

AU - Phetsouvanh, Rattanaphone

AU - Dittrich, Sabine

AU - Panyanivong, Phonepasith

AU - Paris, Daniel

AU - Newton, Paul

AU - Richards, Allen

AU - Pearson, Talima R

PY - 2018/9/1

Y1 - 2018/9/1

N2 - Orientia tsutsugamushi, formerly Rickettsia tsutsugamushi, is an obligate intracellular pathogen that causes scrub typhus, an underdiagnosed acute febrile disease with high morbidity. Scrub typhus is transmitted by the larval stage (chigger) of Leptotrombidium mites and is irregularly distributed across endemic regions of Asia, Australia and islands of the western Pacific Ocean. Previous work to understand population genetics in O. tsutsugamushi has been based on sub-genomic sampling methods and whole-genome characterization of two genomes. In this study, we compared 40 genomes from geographically dispersed areas and confirmed patterns of extensive homologous recombination likely driven by transposons, conjugative elements and repetitive sequences. High rates of lateral gene transfer (LGT) among O. tsutsugamushi genomes appear to have effectively eliminated a detectable clonal frame, but not our ability to infer evolutionary relationships and phylogeographical clustering. Pan-genomic comparisons using 31 082 high-quality bacterial genomes from 253 species suggests that genomic duplication in O. tsutsugamushi is almost unparalleled. Unlike other highly recombinant species where the uptake of exogenous DNA largely drives genomic diversity, the pan-genome of O. tsutsugamushi is driven by duplication and divergence. Extensive gene innovation by duplication is most commonly attributed to plants and animals and, in contrast with LGT, is thought to be only a minor evolutionary mechanism for bacteria. The near unprecedented evolutionary characteristics of O. tsutsugamushi, coupled with extensive intra-specific LGT, expand our present understanding of rapid bacterial evolutionary adaptive mechanisms.

AB - Orientia tsutsugamushi, formerly Rickettsia tsutsugamushi, is an obligate intracellular pathogen that causes scrub typhus, an underdiagnosed acute febrile disease with high morbidity. Scrub typhus is transmitted by the larval stage (chigger) of Leptotrombidium mites and is irregularly distributed across endemic regions of Asia, Australia and islands of the western Pacific Ocean. Previous work to understand population genetics in O. tsutsugamushi has been based on sub-genomic sampling methods and whole-genome characterization of two genomes. In this study, we compared 40 genomes from geographically dispersed areas and confirmed patterns of extensive homologous recombination likely driven by transposons, conjugative elements and repetitive sequences. High rates of lateral gene transfer (LGT) among O. tsutsugamushi genomes appear to have effectively eliminated a detectable clonal frame, but not our ability to infer evolutionary relationships and phylogeographical clustering. Pan-genomic comparisons using 31 082 high-quality bacterial genomes from 253 species suggests that genomic duplication in O. tsutsugamushi is almost unparalleled. Unlike other highly recombinant species where the uptake of exogenous DNA largely drives genomic diversity, the pan-genome of O. tsutsugamushi is driven by duplication and divergence. Extensive gene innovation by duplication is most commonly attributed to plants and animals and, in contrast with LGT, is thought to be only a minor evolutionary mechanism for bacteria. The near unprecedented evolutionary characteristics of O. tsutsugamushi, coupled with extensive intra-specific LGT, expand our present understanding of rapid bacterial evolutionary adaptive mechanisms.

KW - adaptive evolution

KW - gene divergence

KW - genome adaptation

KW - lateral gene transfer

KW - pan-genome

KW - scrub typhus

UR - http://www.scopus.com/inward/record.url?scp=85055776989&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85055776989&partnerID=8YFLogxK

U2 - 10.1099/mgen.0.000199

DO - 10.1099/mgen.0.000199

M3 - Article

VL - 4

JO - Microbial genomics

JF - Microbial genomics

SN - 2057-5858

IS - 9

ER -