It's cheap to be colorful

Pigments homologous to the green fluorescent protein (GFP) contribute up to ∼ 14% of the soluble protein content of many anthozoans. Maintenance of such high tissue levels poses a severe energetic penalty to the animals if protein turnover is fast. To address this as yet unexplored issue, we established that the irreversible green‐to‐red conversion of the GFP‐like pigments from the reef corals Montastrea cavernosa (mcavRFP) and Lobophyllia hemprichii (EosFP) is driven by violet–blue radiation in vivo and in situ. In the absence of photoconverting light, we subsequently tracked degradation of the red‐converted forms of the two proteins in coral tissue using in vivo spectroscopy and immunochemical detection of the post‐translational peptide backbone modification. The pigments displayed surprisingly slow decay rates, characterized by half‐lives of ∼ 20 days. The slow turnover of GFP‐like proteins implies that the associated energetic costs for being colorful are comparatively low. Moreover, high in vivo stability makes GFP‐like proteins suitable for functions requiring high pigment concentrations, such as photoprotection.

[1]  Thomas W. Cronin,et al.  Biological properties of coral GFP-type proteins provide clues for engineering novel optical probes and biosensors , 2004, SPIE BiOS.

[2]  G. Phillips,et al.  The molecular structure of green fluorescent protein , 1996, Nature Biotechnology.

[3]  J. Wiedenmann,et al.  EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Mark Prescott,et al.  The 2.0-Å Crystal Structure of eqFP611, a Far Red Fluorescent Protein from the Sea Anemone Entacmaea quadricolor* , 2003, Journal of Biological Chemistry.

[5]  N. Marshall,et al.  Are Corals Colorful? , 2006, Photochemistry and photobiology.

[6]  M. Chalfie GREEN FLUORESCENT PROTEIN , 1995, Photochemistry and photobiology.

[7]  C. Tyler-Smith,et al.  Attenuation of green fluorescent protein half-life in mammalian cells. , 1999, Protein engineering.

[8]  A. Miyawaki,et al.  An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. W. Young Solar radiation and age-related macular degeneration. , 1988, Survey of ophthalmology.

[10]  Atsushi Miyawaki,et al.  Green fluorescent protein-like proteins in reef Anthozoa animals. , 2002, Cell structure and function.

[11]  J. Wiedenmann,et al.  The morphs of Anemonia aff. sulcata (Cnidaria, Anthozoa) in particular consideration of the ectodermal pigments , 1999 .

[12]  Konstantin A Lukyanov,et al.  zFP538, a yellow-fluorescent protein from Zoanthus, contains a novel three-ring chromophore. , 2005, Biochemistry.

[13]  P. Falkowski,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Green-fluorescent proteins in Caribbean corals , 2022 .

[14]  W. Ward Biochemical and physical properties of green fluorescent protein. , 2005, Methods of biochemical analysis.

[15]  Roger Y Tsien,et al.  Recent advances in technology for measuring and manipulating cell signals , 2000, Current Opinion in Neurobiology.

[16]  G. Ulrich Nienhaus,et al.  Photoconvertible Fluorescent Protein EosFP: Biophysical Properties and Cell Biology Applications , 2006, Photochemistry and photobiology.

[17]  Guy Cox,et al.  Photoinduced activation of GFP-like proteins in tissues of reef corals , 2006, SPIE BiOS.

[18]  J. Wiedenmann,et al.  Live-cell imaging with EosFP and other photoactivatable marker proteins of the GFP family , 2006, Expert review of proteomics.

[19]  J. Wiedenmann,et al.  Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Exploring chromophore--protein interactions in fluorescent protein cmFP512 from Cerianthus membranaceus: X-ray structure analysis and optical spectroscopy. , 2006, Biochemistry.

[21]  M. Matz,et al.  Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). , 2003, Molecular biology and evolution.

[22]  A. Salih,et al.  Simultaneous Time Resolution of the Emission Spectra of Fluorescent Proteins and Zooxanthellar Chlorophyll in Reef-building Corals¶,† , 2003, Photochemistry and photobiology.

[23]  Guy Cox,et al.  Fluorescent pigments in corals are photoprotective , 2000, Nature.

[24]  Michael P Lesser,et al.  Quenching of superoxide radicals by green fluorescent protein. , 2006, Biochimica et biophysica acta.

[25]  I. Vorobjev,et al.  Blue Light Inhibits Mitosis in Tissue Culture Cells , 1998, Bioscience reports.

[26]  B. Vallone,et al.  Chromophore-protein interactions in the anthozoan green fluorescent protein asFP499. , 2006, Biophysical journal.

[27]  O. Hoegh‐Guldberg,et al.  The 2.2 A crystal structure of a pocilloporin pigment reveals a nonplanar chromophore conformation. , 2003, Structure.

[28]  O. Hoegh-Guldberg,et al.  Major colour patterns of reef-building corals are due to a family of GFP-like proteins , 2001, Coral Reefs.

[29]  S. Lukyanov,et al.  Fluorescent proteins from nonbioluminescent Anthozoa species , 1999, Nature Biotechnology.

[30]  川口 四郎 On the physiology of reef corals 4 : study on the pigments , 1943 .

[31]  G Ulrich Nienhaus,et al.  A far-red fluorescent protein with fast maturation and reduced oligomerization tendency from Entacmaea quadricolor (Anthozoa, Actinaria) , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S J Remington,et al.  Refined crystal structure of DsRed, a red fluorescent protein from coral, at 2.0-A resolution. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  K. Spindler,et al.  Cracks in the beta-can: fluorescent proteins from Anemonia sulcata (Anthozoa, Actinaria). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  K. Lukyanov,et al.  Diversity and evolution of the green fluorescent protein family , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  S. Lukyanov,et al.  GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. , 2004, Molecular biology and evolution.

[36]  Franz Oswald,et al.  Identification of GFP-like Proteins in Nonbioluminescent, Azooxanthellate Anthozoa Opens New Perspectives for Bioprospecting , 2004, Marine Biotechnology.

[37]  S. Lukyanov,et al.  Natural Animal Coloration Can Be Determined by a Nonfluorescent Green Fluorescent Protein Homolog* , 2000, The Journal of Biological Chemistry.

[38]  Konstantin A Lukyanov,et al.  Far-red fluorescent tag for protein labelling. , 2002, The Biochemical journal.

[39]  Atsushi Miyawaki,et al.  Photo-induced peptide cleavage in the green-to-red conversion of a fluorescent protein. , 2003, Molecular cell.

[40]  J. Wiedenmann,et al.  A green to red photoconvertible protein as an analyzing tool for early vertebrate development , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  Anya Salih,et al.  Contributions of host and symbiont pigments to the coloration of reef corals , 2007, The FEBS journal.