Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella

Alexander Harms, Francisca H.I.D. Segers, Maxime Quebatte, Claudia Mistl, Pablo Manfredi, Jonas Körner, Bruno B Chomel, Michael Kosoy, Soichi Maruyama, Philipp Engel, Christoph Dehio

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The α-proteobacterial genus Bartonella comprises a group of ubiquitous mammalian pathogens that are studied as a model for the evolution of bacterial pathogenesis. Vast abundance of two particular phylogenetic lineages of Bartonella had been linked to enhanced host adaptability enabled by lineage-specific acquisition of a VirB/D4 type IV secretion system (T4SS) and parallel evolution of complex effector repertoires. However, the limited availability of genome sequences from one of those lineages as well as other, remote branches of Bartonella has so far hampered comprehensive understanding of how the VirB/D4 T4SS and its effectors called Beps have shaped Bartonella evolution. Here, we report the discovery of a third repertoire of Beps associated with the VirB/D4 T4SS of B. ancashensis, a novel human pathogen that lacks any signs of host adaptability and is only distantly related to the two species-rich lineages encoding a VirB/D4 T4SS. Furthermore, sequencing of ten new Bartonella isolates from under-sampled lineages enabled combined in silico analyses and wet lab experiments that suggest several parallel layers of functional diversification during evolution of the three Bep repertoires from a single ancestral effector. Our analyses show that the Beps of B. ancashensis share many features with the two other repertoires, but may represent a more ancestral state that has not yet unleashed the adaptive potential of such an effector set. We anticipate that the effectors of B. ancashensis will enable future studies to dissect the evolutionary history of Bartonella effectors and help unraveling the evolutionary forces underlying bacterial host adaptation.

Original languageEnglish (US)
Pages (from-to)761-776
Number of pages16
JournalGenome Biology and Evolution
Volume9
Issue number3
DOIs
StatePublished - Mar 1 2017

Fingerprint

Bartonella
secretion
pathogen
parallel evolution
genome
phylogenetics
pathogens
history
Computer Simulation
type IV secretion system
Type IV Secretion Systems
pathogenesis
experiment
History
Genome
phylogeny

Keywords

  • AMPylation
  • bacterial effector
  • filamentation induced by cAMP
  • parallel evolution

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella. / Harms, Alexander; Segers, Francisca H.I.D.; Quebatte, Maxime; Mistl, Claudia; Manfredi, Pablo; Körner, Jonas; Chomel, Bruno B; Kosoy, Michael; Maruyama, Soichi; Engel, Philipp; Dehio, Christoph.

In: Genome Biology and Evolution, Vol. 9, No. 3, 01.03.2017, p. 761-776.

Research output: Contribution to journalArticle

Harms, A, Segers, FHID, Quebatte, M, Mistl, C, Manfredi, P, Körner, J, Chomel, BB, Kosoy, M, Maruyama, S, Engel, P & Dehio, C 2017, 'Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella', Genome Biology and Evolution, vol. 9, no. 3, pp. 761-776. https://doi.org/10.1093/gbe/evx042
Harms, Alexander ; Segers, Francisca H.I.D. ; Quebatte, Maxime ; Mistl, Claudia ; Manfredi, Pablo ; Körner, Jonas ; Chomel, Bruno B ; Kosoy, Michael ; Maruyama, Soichi ; Engel, Philipp ; Dehio, Christoph. / Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella. In: Genome Biology and Evolution. 2017 ; Vol. 9, No. 3. pp. 761-776.
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