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Journal of Bacteriology, April 2004, p. 2439-2448, Vol. 186, No. 8
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.8.2439-2448.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Expression Islands Clustered on the Symbiosis Island of the Mesorhizobium loti Genome

Toshiki Uchiumi,1 Takuji Ohwada,2 Manabu Itakura,3 Hisayuki Mitsui,3 Noriyuki Nukui,3 Pramod Dawadi,3 Takakazu Kaneko,4 Satoshi Tabata,4 Tadashi Yokoyama,5 Kouhei Tejima,5 Kazuhiko Saeki,6 Hirofumi Omori,6 Makoto Hayashi,7 Takaki Maekawa,7 Rutchadaporn Sriprang,7 Yoshikatsu Murooka,7 Shigeyuki Tajima,8 Kenshiro Simomura,8 Mika Nomura,8 Akihiro Suzuki,1 Yoshikazu Shimoda,1 Kouki Sioya,1 Mikiko Abe,1 and Kiwamu Minamisawa3*

Department of Chemistry and BioScience, Faculty of Science, Kagoshima University, Kagoshima 890-0065,1 Department of Agricultural and Life Sciences, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555,2 Graduate School of Life Sciences, Tohoku University, Aoba-ku, Sendai 980-8577,3 Kazusa DNA Research Institute, 2-6-7 Kazusa-Kamatari, Chiba 292-0812,4 Tokyo University of Agriculture and Technology, Saiwaicho, Fuchu 183-8509, Tokyo,5 Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043,6 Department of Biotechnology, Graduate School of Engineering, Osaka University, Suita, Osaka 565-0871,7 Department of Life Science, Kagawa University, Miki-cho, Kagawa 761-0795, Japan8

Received 11 November 2003/ Accepted 12 January 2004

Rhizobia are symbiotic nitrogen-fixing soil bacteria that are associated with host legumes. The establishment of rhizobial symbiosis requires signal exchanges between partners in microaerobic environments that result in mutualism for the two partners. We developed a macroarray for Mesorhizobium loti MAFF303099, a microsymbiont of the model legume Lotus japonicus, and monitored the transcriptional dynamics of the bacterium during symbiosis, microaerobiosis, and starvation. Global transcriptional profiling demonstrated that the clusters of genes within the symbiosis island (611 kb), a transmissible region distinct from other chromosomal regions, are collectively expressed during symbiosis, whereas genes outside the island are downregulated. This finding implies that the huge symbiosis island functions as clustered expression islands to support symbiotic nitrogen fixation. Interestingly, most transposase genes on the symbiosis island were highly upregulated in bacteroids, as were nif, fix, fdx, and rpoN. The genome region containing the fixNOPQ genes outside the symbiosis island was markedly upregulated as another expression island under both microaerobic and symbiotic conditions. The symbiosis profiling data suggested that there was activation of amino acid metabolism, as well as nif-fix gene expression. In contrast, genes for cell wall synthesis, cell division, DNA replication, and flagella were strongly repressed in differentiated bacteroids. A highly upregulated gene in bacteroids, mlr5932 (encoding 1-aminocyclopropane-1-carboxylate deaminase), was disrupted and was confirmed to be involved in nodulation enhancement, indicating that disruption of highly expressed genes is a useful strategy for exploring novel gene functions in symbiosis.

* Corresponding author. Mailing address: Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan. Phone: 81-22-217-5684. Fax: 81-22-217-5684. E-mail: kiwamu{at}ige.tohoku.ac.jp.

Journal of Bacteriology, April 2004, p. 2439-2448, Vol. 186, No. 8
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.8.2439-2448.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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