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The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae
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.
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2004 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 101, no 26, 9716-9721 p.Article in journal (Refereed) Published
Abstract [en]

We present the complete genomes of two human pathogens, Bartonella quintana (1,581,384 bp) and Bartonella henselae (1,931,047 bp). The two pathogens maintain several similarities in being transmitted by insect vectors, using mammalian reservoirs, infecting similar cell types (endothelial cells and erythrocytes) and causing vasculoproliferative changes in immunocompromised hosts. A primary difference between the two pathogens is their reservoir ecology. Whereas B. quintana is a specialist, using only the human as a reservoir, B. henselae is more promiscuous and is frequently isolated from both cats and humans. Genome comparison elucidated a high degree of overall similarity with major differences being B. henselae specific genomic islands coding for filamentous hemagglutinin, and evidence of extensive genome reduction in B. quintana, reminiscent of that found in Rickettsia prowazekii. Both genomes are reduced versions of chromosome I from the highly related pathogen Brucella melitensis. Flanked by two rRNA operons is a segment with similarity to genes located on chromosome II of B. melitensis, suggesting that it was acquired by integration of megareplicon DNA in a common ancestor of the two Bartonella species. Comparisons of the vector-host ecology of these organisms suggest that the utilization of host-restricted vectors is associated with accelerated rates of genome degradation and may explain why human pathogens transmitted by specialist vectors are outnumbered by zoonotic agents, which use vectors of broad host ranges.

Place, publisher, year, edition, pages
2004. Vol. 101, no 26, 9716-9721 p.
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-91600DOI: 10.1073/pnas.0305659101OAI: oai:DiVA.org:uu-91600DiVA: diva2:164391
Available from: 2004-04-13 Created: 2004-04-13 Last updated: 2017-12-14Bibliographically approved
In thesis
1. Mitochondrial Evolution: Turning Bugs into Features
Open this publication in new window or tab >>Mitochondrial Evolution: Turning Bugs into Features
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The bacterial origin of mitochondria from an ancient endosymbiosis is now widely accepted and the mitochondrial ancestor is generally believed to belong to the bacterial subdivision α-proteobacteria. The high fraction of mitochondrial proteins encoded in the nucleus has commonly been explained with a massive transfer of genes from the genome of the ancestral mitochondrion.

The aim of this work was to get a better understanding of the mitochondrial origin and evolution by comparative genomics and phylogenetic analyses on mitochondria and α-proteobacteria. To this end, we sequenced the genomes of the intracellular parasites Bartonella henselae and Bartonella quintana, the causative agents of cat-scratch disease and trench fever, and compared them with other α-proteobacteria as well as mitochondrial eukaryotes.

Our results suggest that the adaptation to an intracellular life-style is coupled to an increased rate of genome degradation and a reduced ability to accommodate environmental changes. Reconstruction of the α-proteobacterial ancestor and phylogenetic analyses of the mitochondrial proteome in yeast revealed that only a small fraction of the proteins used for mitochondrial functions could be traced to the α-proteobacteria. Furthermore, a substantial fraction of the mitochondrial proteins was of eukaryotic origin and while most of the genes of the α-proteobacterial ancestor have been lost, many of those that have been transferred to the nuclear genome seem to encode non-mitochondrial proteins.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2004. 37 p.
Series
Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1104-232X ; 961
Keyword
Biology, Biologi
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-4216 (URN)91-554-5933-1 (ISBN)
Public defence
2004-05-14, Ekmansalen, Kärnhuset, EBC, Uppsala, 13:15
Opponent
Supervisors
Available from: 2004-04-13 Created: 2004-04-13Bibliographically approved
2. Lifestyle and Genome Evolution in Vector-Borne Bacteria: A Comparison of Three Bartonella Species
Open this publication in new window or tab >>Lifestyle and Genome Evolution in Vector-Borne Bacteria: A Comparison of Three Bartonella Species
2005 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Livsstil och genomevolution i vektorburna bakterier : en jämförelse av tre Bartonella-arter
Abstract [en]

Bacterial genomes provide records of the molecular processes associated with emergence and evolution of different bacterial lifestyles. This thesis is based on whole-genome comparisons within the genus Bartonella, an excellent model system for studies of host- and vector-specificity and infection outcome in animal-associated bacteria. The louse-borne human specialist and trench fever agent Bartonella quintana was contrasted to the flea-borne generalist relatives Bartonella henselae and Bartonella grahamii, which cause asymptomatic infection in cat and mouse respectively. While B. henselae is commonly isolated from humans, and causes cat scratch disease, there is only one reported case of B. grahamii human infection.

The gene complements of the three species are nested like Russian dolls with the smaller genome (B. quintana) being entirely contained in the medium sized (B. henselae), which in turned is contained in the largest (B. grahamii). Size differences reflect differences in the horizontally and vertically acquired gene content, and in the number of genus- and species- specific genes, owing to differential impact of bacteriophages and plasmids, and to different degrees of genome decay. These processes can be attributed to the three distinct lifestyles.

Comparisons with other alpha-proteobacteria suggest that the Bartonella genus as a whole evolved from plant-associated species, and that horizontal transfer, in particular of genes involved in interaction with the host, played a key role in the transition to animal intracellular lifestyle. The long-term genome decay associated with this lifestyle is most advanced in the host-restricted B. quintana. The broad host-range species B. grahamii has the largest genome and the largest proportion of auxiliary DNA of the three, probably because it has access to a larger gene pool. In encodes all the known pathogenicity determinants found in the genomes of B. henselae and B. quintana, suggesting that these genes primarily evolved to facilitate colonization in the reservoir host.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2005. 57 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 87
Keyword
Biology, Bartonella, evolution, host-restriction, vector-borne, horizontal gene transfer, genome reduction, alpha-proteobacteria, Type-IV secretion, Biologi
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-5913 (URN)91-554-6326-6 (ISBN)
Public defence
2005-09-30, Zootissalen, Evolutionsbiologiskt centrum, Villavägen 9, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2005-09-09 Created: 2005-09-09 Last updated: 2009-08-04Bibliographically approved

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Alsmark, Cecilia M.Frank, A. CarolinArdell, David H.Eriksson, Ann-SofieHolmberg, MartinAndersson, Siv G. E.

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