MBE Advance Access published online on October 25, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp252
Research Article |
Vertebrate Rhodopsin Adaptation to Dim Light via Rapid Meta-II Intermediate Formation
1 Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
2 Department of Cellular and Molecular Biology, Molecular Biology Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
3 Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto 606-8502 Japan
4 Present address: sugawarat@pri.kyoto-u.ac.jp, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
Corresponding authors: N. Okada, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan, nokada{at}bio.titech.ac.jp, Tel: 81-45-924-5742, Fax: 81-45-924-5835
H. Imai, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan, imai{at}pri.kyoto-u.ac.jp, Tel: 81-568-63-0577, Fax: 81-568-62-9557
Received for publication March 10, 2009. Revision received June 30, 2009. Revision received August 27, 2009. Revision received September 27, 2009. Accepted for publication October 1, 2009.
Rhodopsin is a photoreceptive protein present in vertebrate rod photoreceptor cells, which are responsible for scotopic vision. Recent molecular studies have shown that several aquatic vertebrate species have independently acquired rhodopsin containing Asp83Asn, Glu122Gln and Ala292Ser substitutions, causing a blue-shift in the rhodopsin absorption spectra for adaptation to the blue-green photic environment in deep water. Here, we provide new evidence for the evolutionary and functional relevance of the Asp83Asn substitution. Spectroscopic and kinetic analyses of rhodopsins in six cichlid fishes from the East African Great Lakes using charge-coupled device spectrophotometer revealed that the Asp83Asn substitution accelerated formation of meta-II, a rhodopsin intermediate crucial for activation of the G-protein transducin. Because rapid formation of meta-II likely results in effective transduction of photic signals, it is reasonable to assume that deep-water cichlid species have acquired rhodopsin containing Asn83 to adapt to dim lighting. Remarkably, rhodopsin containing Asn83 has been identified in terrestrial vertebrates such as bats, and these rhodopsin variants also exhibit accelerated meta-II formation. Our results indicated that the Asp83Asn substitution observed in a variety of animal species was acquired independently in many different lineages during vertebrate evolution for adaptation to dimly lit environments.
Key Words: cichlid • rhodopsin • meta-II • bat