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Evolution of Host Adaptation Systems in  the Mammalian Blood Specialist Bartonella
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution. (Molecular Evolution)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution. (Molecular Evolution)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution. (Molecular Evolution)
School of Biotechnology, Royal Institute of Technology.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Bacteria of the genus Bartonella are facultative intracellular bacteria infecting the red blood cells of mammals. Bartonella isolates have now been reported from a wide range of mammalian host species, including humans, domestic animals such as pets and livestock, as well as many wild animals such as deer, moose, kangaroo, and whales. Here, we present the first major genus-wide investigation of host-adaptation systems in Bartonella, using 5 published and 5 draft genome sequences. The sampling includes both clinical and natural isolates, and represent well the major phylogenetic diversity of the genus. Our study reveals four distinct protein families of Type V Secretion Systems (T5SS) shared by all sequenced members of the genus. We also show that a recently identified gene transfer agent (GTA) consisting of a defective phage is, surprisingly, the most conserved gene cluster among all Bartonella-specific or imported genes, strongly emphasizing the functional importance of this system for the life-style and evolution of Bartonella.

Keyword [en]
host adaptation, pathogen, secretion systems, flagella, gene transfer agent, evolution
National Category
Bioinformatics and Systems Biology
Research subject
Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-107784OAI: oai:DiVA.org:uu-107784DiVA: diva2:232918
Available from: 2009-08-26 Created: 2009-08-26 Last updated: 2010-01-14
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
2. Genome Evolution and Host Adaptation in Bartonella
Open this publication in new window or tab >>Genome Evolution and Host Adaptation in Bartonella
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Bacteria of the genus Bartonella infect the red blood cells of a wide range of wild and domestic mammals and are transmitted between hosts by blood-sucking insects. Although most Bartonella infections are asymptomatic, the genus contains several human pathogens. In this work, host adaptation and host switches in Bartonella have been studied from a genomic perspective, with special focus on the acquisition and evolution of genes involved in host interactions.

As part of this study, the complete genome of B. grahamii isolated from a Swedish wood mouse was sequenced. A genus-wide comparison revealed that rodent-associated Bartonella species, which have rarely been associated with human disease, have the largest genomes and the largest number of host-adaptability genes. Analysis of known and putative genes for host interactions identified several families of autotransporters as horizontally transferred to the Bartonella ancestor, with a possible role both during early host adaptation and subsequent host shifts.

In B. grahamii, the association of a gene transfer agent (GTA) and phage-derived run-off replication of a large genomic segment was demonstrated for the first time. Among all acquisitions to the Bartonella ancestor, the only well conserved gene clusters are those that encode the GTA and contain the origin of the run-off replication. This conservation, along with a high density of host-adaptability genes in the amplified region suggest that the GTA provides a strong selective advantage, possibly by increasing recombination frequencies of host-adaptability genes, thereby facilitating evasion of the host immune system and colonization of new hosts.

B. grahamii displays stronger geographic pattern and higher recombination frequencies than the cat-associated B. henselae, probably caused by different lifestyles and/or population sizes of the hosts. The genomic diversity of B. grahamii is markedly lower in Europe and North America than in Asia, possibly an effect of reduced host variability in these areas following the latest ice age.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2009. 68 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 675
Keyword
Bartonella, genome evolution, genome diversity, phage, gene transfer agent, secretion system, microarray
National Category
Bioinformatics and Systems Biology
Research subject
Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-108376 (URN)978-91-554-7616-8 (ISBN)
Public defence
2009-11-06, Lindahlsalen, EBC, Norbyvägen 18, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2009-10-15 Created: 2009-09-17 Last updated: 2009-10-15Bibliographically approved

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