A green dichromophoric protein enabling foliage mimicry in arthropods
Abstract
Molecular mechanisms underlying the green insect camouflage have puzzled researchers for over a century. Here, we isolated and identified a green water-soluble protein from the integument of bush-cricket Tettigonia cantans . De novo sequencing and cloning revealed a severely fragmented form of vitellogenins, ubiquitous and multifunctional, but still largely enigmatic glycolipoproteins essential for embryonic development and lacking structural characterization. The distinctive color of the identified chromoprotein results from binding of a remarkable combination of farnesylated bilins (recently identified, tentative heme A catabolites) and xanthophylls, which commensurably absorb light in the 600 to 700 nm and 400 to 550 nm spectral regions and thereby produce a hue that perfectly mimics foliage. The high-resolution crystal structure of this unique ~80 kDa dichromophoric protein, which we named “dibilinoxanthinin” (DBXN), revealed two DBXN protomers, each consisting of three polypeptides, with a novel fold enclosing a large hydrophobic cavity that accommodates two bilins, two luteins, and four phosphatidylcholines, all anchored by hydrogen bonds and giving DBXN unique biochemical and optical properties. Among the green insects tested, some contained yellow and blue chromophores in separate fractions, while others had green proteins similar to DBXN, although not necessarily of the same size. Surprisingly, we isolated and identified a larger vitellogenin proteoform with DBXN-like absorption, from the green huntsman spider Micrommata virescens . These data illustrate striking variations in the DBXN-related pigmentation mechanism among different green arthropods and suggest that vitellogenins may have undergone neofunctionalization, reflecting their potential for functional diversification.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (13)
Nikita A. Egorkin
Laboratory of Protein–Protein Interactions, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Anatoly M. Aleksin
Laboratory of Protein–Protein Interactions, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Ilya A. Sedlov
Laboratory of Protein–Protein Interactions, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Nikita I. Zhiganov
Department of Entomology, School of Biology, M.V. Lomonosov Moscow State University
Daria V. Bodunova
Department of Biophysics, School of Biology, M.V. Lomonosov Moscow State University
Larisa A. Varfolomeeva
Laboratory of Enzyme Engineering, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Yury B. Slonimskiy
Laboratory of Protein–Protein Interactions, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Rustam H. Ziganshin
Group of Mass Spectrometry, Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Vladimir O. Popov
Laboratory of Enzyme Engineering, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Konstantin M. Boyko
Laboratory of Enzyme Engineering, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences
Alexander A. Vassilevski
Laboratory of Molecular Instruments for Neurobiology, Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Eugene G. Maksimov
Department of Biophysics, School of Biology, M.V. Lomonosov Moscow State University
Nikolai N. Sluchanko
Laboratory of Protein–Protein Interactions, A.N. Bach Institute of Biochemistry, Federal Research Center of Biotechnology, Russian Academy of Sciences