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Eukaryotic Cell, December 2007, p. 2419-2428, Vol. 6, No. 12
1535-9778/07/$08.00+0     doi:10.1128/EC.00204-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Regulation of Ammonia Homeostasis by the Ammonium Transporter AmtA in Dictyostelium discoideum

Ryuji Yoshino,^1,5* Takahiro Morio,¹ Yoko Yamada,^2, Hidekazu Kuwayama,^1,3 Masazumi Sameshima,^2,4 Yoshimasa Tanaka,¹ Hiromi Sesaki,⁵ and Miho Iijima^5*

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan 305-8572,¹ Electron Microscopy Center, The Tokyo Metropolitan Institute of Medical Science, Bunkyo-ku, Tokyo, Japan 113-8613,² Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka, Japan 565-0871,³ Department of Biofunctional Science Faculty of Agriculture and Life Science, Hirosaki University, Bunkyo-cho, Hirosaki, Aomori, Japan 036-8561,⁴ Department of Cell Biology, Johns Hopkins University, School of Medicine, Baltimore, Maryland 21205⁵

Received 11 June 2007/ Accepted 3 October 2007

Ammonia has been shown to function as a morphogen at multiple steps during the development of the cellular slime mold Dictyostelium discoideum; however, it is largely unknown how intracellular ammonia levels are controlled. In the Dictyostelium genome, there are five genes that encode putative ammonium transporters: amtA, amtB, amtC, rhgA, and rhgB. Here, we show that AmtA regulates ammonia homeostasis during growth and development. We found that cells lacking amtA had increased levels of ammonia/ammonium, whereas their extracellular ammonia/ammonium levels were highly decreased. These results suggest that AmtA mediates the excretion of ammonium. In support of a role for AmtA in ammonia homeostasis, AmtA mRNA is expressed throughout the life cycle, and its expression level increases during development. Importantly, AmtA-mediated ammonia homeostasis is critical for many developmental processes. amtA^– cells are more sensitive to NH₄Cl than wild-type cells in inhibition of chemotaxis toward cyclic AMP and of formation of multicellular aggregates. Furthermore, even in the absence of exogenously added ammonia, we found that amtA^– cells produced many small fruiting bodies and that the viability and germination of amtA^– spores were dramatically compromised. Taken together, our data clearly demonstrate that AmtA regulates ammonia homeostasis and plays important roles in multiple developmental processes in Dictyostelium.

Published ahead of print on 19 October 2007.

Present address: University of Dundee, MSI/WTB Complex, Dow Street, Dundee DD1 5EH, United Kingdom.