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Diversifying Selection and Concerted Evolution of a Type IV Secretion System in Bartonella
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
2008 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 25, no 2, 287-300 p.Article in journal (Refereed) Published
Abstract [en]

We have studied the evolution of a type TV secretion system (T4SS), in Bartonella, which is thought to have changed function from conjugation to erythrocyte adherence following a recent horizontal gene transfer event. The system, called Trw, is unique among T4SSs in that genes encoding both exo- and intracellular components are located within the same duplicated fragment. This provides an opportunity to study the influence of selection on proteins involved in host-pathogen interactions. We sequenced the trw locus from several strains of Bartonella henselae and investigated its evolutionary history by comparisons to other Bartonella species. Several instances of recombination and gene conversion events where detected in the 2- to 5-fold duplicated gene fragments encompassing trwJIH, explaining the homogenization of the anchoring protein TrwI and the divergence of the minor pilus protein TrwJ. A phylogenetic analysis of the 7- to 8-fold duplicated gene coding for the major pilus protein TrwL displayed 2 distinct clades, likely representing a subfunctionalization event. The analyses of the B. henselae strains also identified a recent horizontal transfer event of almost the complete trwL region. We suggest that the switch in function of the T4SS was mediated by the duplication of the genes encoding pilus components and their diversification by combinatorial sequence shuffling within and among genomes. We suggest that the pilus proteins have evolved by diversifying selection to match a divergent set of erythrocyte surface structures, consistent with the trench warfare coevolutionary model.

Place, publisher, year, edition, pages
2008. Vol. 25, no 2, 287-300 p.
Keyword [en]
type IV secretion system, Bartonella, duplication, recombination, gene conversion, host-pathogen interaction
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-14988DOI: 10.1093/molbev/msm252ISI: 000253634800007PubMedID: 18065487OAI: oai:DiVA.org:uu-14988DiVA: diva2:42759
Available from: 2008-02-01 Created: 2008-02-01 Last updated: 2017-12-11Bibliographically approved
In thesis
1. Evolutionary Processes and Genome Dynamics in Host-Adapted Bacteria
Open this publication in new window or tab >>Evolutionary Processes and Genome Dynamics in Host-Adapted Bacteria
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Many bacteria live in close association with other organisms such as plants and animals, with important implications for both health and disease. This thesis investigates bacteria that are well adapted to live inside an animal host, and describes the molecular evolutionary processes underlying host-adaptation, based on bacterial genome comparisons.

Insect-transmitted bacteria of the genus Bartonella infect the red blood cells of mammals, and we investigate host adaptation and genome evolution in this genus. In Bartonella, many host-interaction systems are encoded in a highly variable chromosomal segment previously shown to be amplified and packaged into bacteriophage particles. Among all genes imported into the Bartonella ancestor, we identify the short gene cluster encoding these phage particles as the most evolutionary conserved, indicating a strong selective advantage and a role in niche adaptation. We also provide an overview of the remarkable evolutionary dynamics of type IV and type V secretion systems, including a detailed analysis of the type IV secretion system trw. Our results highlight the importance of recombination and gene conversion in the evolution of host-adaptation systems, and reveal how these mutational mechanisms result in strikingly different outcomes depending on the selective constraints.

In the insect endosymbionts Buchnera and Blochmannia, we show that genes frameshifted at poly(A) tracts can remain functional due to transcriptional slippage. Selection against poly(A) tracts is very inefficient in these genomes compared to other bacteria, and we discuss why this can lead to increased rates of gene loss. Using the human pathogen Helicobacter pylori as a model, we provide a deeper understanding of why highly expressed genes evolve slowly.

This thesis emphasizes the power of using complete genome sequences to study evolutionary processes. In particular, we argue that knowledge about the complex evolution of duplicated gene segments is crucial to understand host adaptation in bacteria.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2009. 64 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 668
Keyword
molecular evolution, pathogen, secretion system, Bartonella, Buchnera, Blochmannia, Helicobacter
National Category
Bioinformatics and Systems Biology
Research subject
Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-107720 (URN)978-91-554-7596-3 (ISBN)
Public defence
2009-10-09, Lindahlsalen, EBC, Norbyvägen 18, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2009-09-18 Created: 2009-08-24 Last updated: 2009-09-22

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Nystedt, BjörnThollesson, MikaelAndersson, Siv

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