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Journal of Bacteriology, August 2004, p. 5138-5146, Vol. 186, No. 15
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.15.5138-5146.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

DNA Microarray Analysis of Genome Dynamics in Yersinia pestis: Insights into Bacterial Genome Microevolution and Niche Adaptation

Dongsheng Zhou,^1, Yanping Han,^1, Yajun Song,¹ Zongzhong Tong,² Jin Wang,¹ Zhaobiao Guo,¹ Decui Pei,¹ Xin Pang,¹ Junhui Zhai,¹ Min Li,³ Baizhong Cui,³ Zhizhen Qi,³ Lixia Jin,³ Ruixia Dai,³ Zongmin Du,¹ Jingyue Bao,² Xiuqing Zhang,² Jun Yu,² Jian Wang,² Peitang Huang,¹ and Ruifu Yang^1*

Laboratory of Analytical Microbiology, National Centre for Biomedical Analysis, Army Center for Microbial Detection and Research, Institute of Microbiology and Epidemiology, Academy of Military Medical Sciences, Beijing 100071,¹ Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 100101,² Qinghai Institute for Endemic Diseases Prevention and Control, Xining 811602, China³

Received 8 February 2004/ Accepted 31 May 2004

Genomics research provides an unprecedented opportunity for us to probe into the pathogenicity and evolution of the world's most deadly pathogenic bacterium, Yersinia pestis, in minute detail. In our present work, extensive microarray analysis in conjunction with PCR validation revealed that there are considerable genome dynamics, due to gene acquisition and loss, in natural populations of Y. pestis. We established a genomotyping system to group homologous isolates of Y. pestis, based on profiling or gene acquisition and loss in their genomes, and then drew an outline of parallel microevolution of the Y. pestis genome. The acquisition of a number of genomic islands and plasmids most likely induced Y. pestis to evolve rapidly from Yersinia pseudotuberculosis to a new, deadly pathogen. Horizontal gene acquisition also plays a key role in the dramatic evolutionary segregation of Y. pestis lineages (biovars and genomovars). In contrast to selective genome expansion by gene acquisition, genome reduction occurs in Y. pestis through the loss of DNA regions. We also theorized about the links between niche adaptation and genome microevolution. The transmission, colonization, and expansion of Y. pestis in the natural foci of endemic plague are parallel and directional and involve gradual adaptation to the complex of interactions between the environment, the hosts, and the pathogen itself. These adaptations are based on the natural selections against the accumulation of genetic changes within genome. Our data strongly support that the modern plague originated from Yunnan Province in China, due to the arising of biovar orientalis from biovar antiqua rather than mediaevalis.

D.Z. and Y.H. contributed equally to this work.

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