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DNA Research Advance Access published online on May 28, 2008
DNA Research, doi:10.1093/dnares/dsn011
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© The Author 2008. Kazusa DNA Research Institute
The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org

The Whole-genome Sequencing of the Obligate Intracellular Bacterium Orientia tsutsugamushi Revealed Massive Gene Amplification During Reductive Genome Evolution

Keisuke Nakayama1, Atsushi Yamashita2, Ken Kurokawa3, Takuya Morimoto1 {dagger}, Michihiro Ogawa3 {ddagger}, Masahiro Fukuhara4, Hiroshi Urakami5, Makoto Ohnishi6, Ikuo Uchiyama7, Yoshitoshi Ogura8, Tadasuke Ooka1, Kenshiro Oshima2,9, Akira Tamura10, Masahira Hattori9 and Tetsuya Hayashi1,8,*

1 Division of Microbiology, Department of Infectious Diseases, Faculty of Medicine, University of Miyazaki, 5200 Kiyotake, Miyazaki 899-1692, Japan1
2 Kitasato Institute for Life Science, Kitasato University, 5-9-1 Shirogane, Minato-ku Tokyo 108-8641, Japan2
3 Laboratory of Comparative Genomics, Graduate School of Information Science, Nara Institute of Science and Technology, 8916-5 Takayama-cho, Ikoma, Nara 630-0192, Japan3
4 Laboratory of Microbiology, Faculty of Pharmacy, Niigata University of Pharmacy and Applied Life Sciences, 265-1 Higashijima, Akiha-ku, Niigata 956-8603, Japan4
5 Laboratory of Food Microbiology and Food Safety, Faculty of Applied Life Sciences, Niigata University of Pharmacy and Applied Life Sciences, 265-1 Higashijima, Akiha-ku, Niigata 956-8603, Japan5
6 Department of Bacteriology, National Institute for Infectious Diseases, Toyama 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan6
7 National Institute for Basic Biology, National Institutes of Natural Sciences, Nishigonaka 38, Myodaiji, Okazaki 444-8585, Japan7
8 Frontier Science Research Center, University of Miyazaki, 5200 Kiyotake, Miyazaki 899-1692, Japan8
9 Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kasiwanoha, Kashiwa, Chiba, 277-8561, Japan9
10 Niigata University of Pharmacy and Applied Life Sciences, 265-1 Higashijima, Niigata 956-8603, Japan10

Received 19 December 2007 ; accepted 2 May 2008.

Scrub typhus (‘Tsutsugamushi’ disease in Japanese) is a mite-borne infectious disease. The causative agent is Orientia tsutsugamushi, an obligate intracellular bacterium belonging to the family Rickettsiaceae of the subdivision alpha-Proteobacteria. In this study, we determined the complete genome sequence of O. tsutsugamushi strain Ikeda, which comprises a single chromosome of 2 008 987 bp and contains 1967 protein coding sequences (CDSs). The chromosome is much larger than those of other members of Rickettsiaceae, and 46.7% of the sequence was occupied by repetitive sequences derived from an integrative and conjugative element, 10 types of transposable elements, and seven types of short repeats of unknown origins. The massive amplification and degradation of these elements have generated a huge number of repeated genes (1196 CDSs, categorized into 85 families), many of which are pseudogenes (766 CDSs), and also induced intensive genome shuffling. By comparing the gene content with those of other family members of Rickettsiacea, we identified the core gene set of the family Rickettsiaceae and found that, while much more extensive gene loss has taken place among the housekeeping genes of Orientia than those of Rickettsia, O. tsutsugamushi has acquired a large number of foreign genes. The O. tsutsugamushi genome sequence is thus a prominent example of the high plasticity of bacterial genomes, and provides the genetic basis for a better understanding of the biology of O. tsutsugamushi and the pathogenesis of ‘Tsutsugamushi’ disease.

Key words: Orientia tsutsugamushi; genome sequencing; obligate intracellular bacterium; repetitive sequence; IS element; integrative and conjugative element; gene amplification; genome reduction

* To whom correspondence should be addressed. E-mail: thayash{at}med.miyazaki-u.ac.jp

Edited by Katsumi Isono

{dagger} Present address: Biological Science Laboratories, Kao Corporation, 2606 Akabane Ichikai Haga, Tochigi 321-3497, Japan; Graduate School of Information Science, and Nara Institute of Science and Technology, 8916-5 Takayama-cho, Ikoma, Nara 630-0192, Japan

{ddagger} Present address: Office of Biologics I, Pharmaceutical and Medical Devices Agency, 3-3-2 Kasumigaseki, Chiyoda-ku, Tokyo 100-0013, Japan


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