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Bartonella Quintana Is a Genomic Derivative of the Zoonotic Agent Bartonella Henselae

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Bartonella Quintana Is a Genomic Derivative of the Zoonotic Agent Bartonella Henselae The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae Cecilia M. Alsmark*†‡, A. Carolin Frank*†, E. Olof Karlberg*†, Boris-Antoine Legault*, David H. Ardell*§, Bjo¨ rn Canba¨ ck*¶, Ann-Sofie Eriksson*, A. Kristina Na¨ slund*, Scott A. Handley*ʈ, Maxime Huvet*, Bernard La Scola*,**, Martin Holmberg††, and Siv G. E. Andersson*‡‡ *Department of Molecular Evolution, Evolutionary Biology Center, Uppsala University, 752 36 Uppsala, Sweden; and ††Department of Medical Sciences, Section for Infectious Diseases, Uppsala University Hospital, 752 85 Uppsala, Sweden Edited by Stanley Falkow, Stanford University, Stanford, CA, and approved February 19, 2004 (received for review September 4, 2003) We present the complete genomes of two human pathogens, henselae has mainly been studied in human umbilical vein Bartonella quintana (1,581,384 bp) and Bartonella henselae endothelial cells, and internalization has been shown to occur (1,931,047 bp). The two pathogens maintain several similarities in both by conventional phagocytosis and by an invasome-mediated being transmitted by insect vectors, using mammalian reservoirs, mechanism (5). Colonization of endothelial cells is important in infecting similar cell types (endothelial cells and erythrocytes) and both reservoir and incidental mammalian hosts and is considered causing vasculoproliferative changes in immunocompromised essential for the establishment and maintenance of the angio- hosts. A primary difference between the two pathogens is their proliferative lesions (4, 6–8). reservoir ecology. Whereas B. quintana is a specialist, using only Of the 19 described Bartonella species that infect a wide variety the human as a reservoir, B. henselae is more promiscuous and is of domestic and wild animals such as cats, dogs, mice, rats, frequently isolated from both cats and humans. Genome compar- squirrels, deer, and moose, 7 have been associated with human ison elucidated a high degree of overall similarity with major disease (9, 10). Experimental animal infection models suggest differences being B. henselae specific genomic islands coding for that the initial infection in the host is in a yet unknown niche, filamentous hemagglutinin, and evidence of extensive genome from which erythrocytes are periodically seeded (10–12). The reduction in B. quintana, reminiscent of that found in Rickettsia VirB͞VirD type IV secretion system is required at an early stage prowazekii. Both genomes are reduced versions of chromosome I of the infection, possibly for colonization of the primary niche from the highly related pathogen Brucella melitensis. Flanked by (11). Bacteria can persist in mature erythrocytes for several two rRNA operons is a segment with similarity to genes located on weeks, with transmission among hosts being mediated by blood- chromosome II of B. melitensis, suggesting that it was acquired by sucking arthropods. In human infections, B. quintana, but not B. integration of megareplicon DNA in a common ancestor of the two henselae, shows intraerythrocytic presence. The human body Bartonella species. Comparisons of the vector–host ecology of louse (B. quintana), the cat flea (B. henselae), and the sand fly these organisms suggest that the utilization of host-restricted (B. bacilliformis) have all been implicated in the eco- vectors is associated with accelerated rates of genome degradation epidemiology of Bartonella infections. Several Bartonella species, and may explain why human pathogens transmitted by specialist including B. henselae, have been detected by PCR in ticks (13), vectors are outnumbered by zoonotic agents, which use vectors of which feed on a large variety of vertebrate hosts. broad host ranges. The expanding number of species identified, the novel disease symptoms described, and the potential for genetic exchange he genus Bartonella contains three major human pathogens, across species have long-term consequences for the epidemiol- Tall of which are facultative intracellular bacteria. Bartonella ogy and virulence of Bartonella infections. To study the evolution quintana is the causative agent of trench fever, a disease that of closely related vector-borne pathogens with different host affected more than 1 million soldiers during World War I and is preference patterns, we compared the complete genome se- currently reemerging among homeless and alcoholic individuals quence of the louse-borne human specialist B. quintana with that in urban areas (1). The trench fever agent is a human specialist of its close relative, the zoonotic agent B. henselae. Our analysis that is transmitted by the human body louse, Pediculus humanus, suggests that specialization to a single vector and͞or host is which also serves as the vector for the typhus pathogen, Rickettsia associated with the loss of extrachromosomal DNA and phage prowazekii. The agent of Carrio´n’s disease, Bartonella bacillifor- genes, possibly making these species less able to accommodate mis, is likewise a human pathogen specialist. In contrast, Bar- change and invade novel environmental niches. tonella henselae infects both humans and cats; 30–60% of domestic cats in the U.S. are infected with B. henselae. Trans- mission among cats is mediated by the cat flea, Ctenocephalides This paper was submitted directly (Track II) to the PNAS office. felis, and to humans by cat scratches or cat bites (1). Data deposition: The sequences reported in this paper have been deposited in the GenBank Natural B. henselae infections produce no clinical symptoms in database [accession nos. BX897699 (B. henselae) and BX897700 (B. quintana)]. the cat, whereas cat-scratch disease in humans causes disease †C.M.A., A.C.F., and E.O.K. contributed equally to this work. manifestations in lymphatic organs, the skin, the liver, and the ‡Present address: Department of Zoology, Natural History Museum, London SW7 5BD, cardiovascular and the nervous systems (1). B. henselae and B. United Kingdom. quintana are unique among bacterial pathogens in that they may §Present address: Linnaeus Centre for Bioinformatics, Biomedical Center, Uppsala Univer- induce tumor-like lesions of the skin (bacillary angiomatosis), sity, 752 36 Uppsala, Sweden. the liver, and the spleen (bacillary peliosis) in immunocompro- ¶Present address: Department of Microbial Ecology, Lund University, 223 62 Lund, Sweden. mised individuals, predominantly AIDS patients (2, 3). Patho- ʈPresent address: Department of Molecular Microbiology, Washington University School of logical angiogenesis manifested as skin lesions may also be Medicine, St. Louis, MO 63110. induced by B. bacilliformis (verruga peruana). Both B. henselae **Present address: Unite´des Rickettsies, Faculte´deMe´ decine, 133 85 Marseille, France. and B. quintana are able to invade endothelial cells and replicate ‡‡To whom correspondence should be addressed. E-mail: [email protected]. within these cells (4, 5). Adhesion to endothelial cells by B. © 2004 by The National Academy of Sciences of the USA 9716–9721 ͉ PNAS ͉ June 29, 2004 ͉ vol. 101 ͉ no. 26 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0305659101 Downloaded by guest on October 1, 2021 Materials and Methods backbone gene order was preserved. The homologous pairs were Genome Sequencing and Assembly. Starting from single colonies, aligned through their inferred protein translations with CLUST- B. henselae (strain Houston-1; original isolate) and B. quintana ALW (17), using the BLOSUM matrix series and default settings. (strain Toulose) were cultured on blood agar plates at 35°C The CODEML program of the PAML package (v. 3.0) (23) was then ͞ ͞ under 5% CO2 95% air for 5 days. DNA preparation, library used to calculate pairwise dN dS, ratios assuming homogeneity of construction, and sequencing were as described previously (14). selection over codons and transition–transversion bias as a free A total of 36,328 and 22,731 shotgun sequences were obtained parameter (initial estimation value 2). Proteins in repeat families were clustered together by amino from the M13 libraries of B. henselae and B. quintana, respec- Ͼ Ͼ tively. Additionally, 5,469 pUC18 clones and 3,166 PCR products acid identity ( 50% over 50% of the length of the protein) as inferred by BLAST. Sequences with sequence similarities to a from B. henselae and 5,217 pUC18 clones and 2,303 PCR ͞ ͞ products from B. quintana were sequenced. After assembly with functional gene and or an ORF in B. henselae and or B. the PHRED and PHRAP software, physical gaps were closed by quintana but not spanning an entire ORF with initiation and direct sequencing of both ends of gap-covering pUC18 clones as termination codons were considered pseudogenes. Short frag- ments of sequences with sequence similarity to a functional gene well as by long-range PCR by using primers from contig ends. ͞ ͞ The location and order of sequences covering long repeated and or an ORF in the B. henselae and or B. quintana genomes regions in B. henselae were resolved by hybridization of PCR were treated as extensively degraded gene remnants. products to Southern blots of NotI digests separated by pulse- Similarity searches of all B. quintana and B. henselae protein field gel electrophoresis. The organization of these and other sequences against the protein sequences encoded by Bartonella suis chromosomes I and II were made separately by using BLASTP repetitive regions was confirmed by ordinary PCR and long- Ͻ Ϫ20 range PCR by using single locus primers. All ambiguous sites (E 1e ). For B. henselae proteins
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