Multiple origins of green coloration in frogs mediated by a novel biliverdin-binding serpin

Author(s):Show less -

Taboada, Carlos ^{[1, 2, 3, 4]} ; Brunetti, Andres E. ^{[4, 5]} ; Lyra, Mariana L. ^{[6, 7]} ; Fitak, Robert R. ^{[1, 8]} ; Faigon Soverna, Ana ^[2] ; Ron, Santiago R. ^[9] ; Lagorio, Maria G. ^{[3, 10]} ; Haddad, Celio F. B. ^{[6, 7]} ; Lopes, Norberto P. ^[4] ; Johnsen, Sonke ^[1] ; Faivovich, Julian ^{[2, 11]} ; Chemes, Lucia B. ^{[12, 13, 14]} ; Bari, Sara E. ^[3]

Affiliation:Show less -

^[1] Duke Univ, Dept Biol, Durham, NC 27708 - USA

^[2] Consejo Nacl Invest Cient & Tecn CONICET, Museo Argentino Ciencias Nat Bernardino Rivadavia, Div Herpetol, C1405DJR, Buenos Aires, DF - Argentina

^[3] Univ Buenos Aires, Fac Ciencias Exactas & Nat, Inst Quim Fis Mat Medio Ambiente & Energia, Consejo Nacl Invest Cient & Tecn CONICET, C1428EHA, Buenos Aires, DF - Argentina

^[4] Univ Sao Paulo, Fac Ciencias Farmaceut Ribeirao Preto, Dept Ciencias BioMol, Nucleo Pesquisa Prod Nat & Sintet NPPNS, BR-14040903 Ribeirao Preto, SP - Brazil

^[5] Univ Nacl Misiones, Fac Ciencias Exactas, Inst Biol Subtrop CONICET UNaM, Lab Genet Evolut Claudio Juan Bidau, RA-3300 Posadas, Misiones - Argentina

^[6] Univ Estadual Paulista, Dept Biodiversidade, BR-13506900 Rio Claro, SP - Brazil

^[7] Univ Estadual Paulista, Ctr Aquicultura, Inst Biociencias, BR-13506900 Rio Claro, SP - Brazil

^[8] Univ Cent Florida, Dept Biol Genom & Bioinformat Cluster, Orlando, FL 32816 - USA

^[9] Pontificia Univ CatOlica Ecuador, Escuela Biol, Museo Zool, Aptdo 17-01-2184, Quito - Ecuador

^[10] Univ Buenos Aires, Fac Ciencias Exactas & Nat, Dept Quim Inorgan Analit & Quim Fis, C1428EHA, Buenos Aires, DF - Argentina

^[11] Univ Buenos Aires, Fac Ciencias Exactas & Nat, Dept Biodiversidad & Biol Expt, C1428EHA, Buenos Aires, DF - Argentina

^[12] Consejo Nacl Invest Cient & Tecn, Fdn Inst Leloir, C1405BWE, Buenos Aires, DF - Argentina

^[13] Consejo Nacl Invest Cient & Tecn, Inst Invest Bioquim Buenos Aires, C1405BWE, Buenos Aires, DF - Argentina

^[14] Univ Nacl San Martin, Inst Invest Biotecnol, RA-1650 San Martin, Buenos Aires - Argentina

• Document type: Journal article
• Source: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA; v. 117, n. 31, p. 18574-18581, AUG 4 2020.
• Web of Science Citations: 2

Abstract

Many vertebrates have distinctive blue-green bones and other tissues due to unusually high biliverdin concentrations-a phenomenon called chlorosis. Despite its prevalence, the biochemical basis, biology, and evolution of chlorosis are poorly understood. In this study, we show that the occurrence of high biliverdin in anurans (frogs and toads) has evolved multiple times during their evolutionary history, and relies on the same mechanism-the presence of a class of serpin family proteins that bind biliverdin. Using a diverse combination of techniques, we purified these serpins from several species of nonmodel treefrogs and developed a pipeline that allowed us to assemble their complete amino acid and nucleotide sequences. The described proteins, hereafter named biliverdin-binding serpins (BBS), have absorption spectra that mimic those of phytochromes and bacteriophytochromes. Our models showed that physiological concentration of BBS5 fine-tune the color of the animals, providing the physiological basis for crypsis in green foliage even under near-infrared light. Additionally, we found that these BBS5 are most similar to human glycoprotein alpha-1-antitrypsin, but with a remarkable functional diversification. Our results present molecular and functional evidence of recurrent evolution of chlorosis, describe a biliverdin-binding protein in vertebrates, and introduce a function for a member of the serpin superfamily, the largest and most ubiquitous group of protease inhibitors. (AU)

• FAPESP's process: 13/50741-7 - Diversity and conservation of Brazilian amphibians
• Grantee: Célio Fernando Baptista Haddad
• Support type: BIOTA-FAPESP Program - Thematic Grants
• FAPESP's process: 17/23725-1 - Genomic Analysis of Skin Symbiotic Bacteria in Frogs as Potential Source of Volatile Compounds
• Grantee: Andrés Eduardo Brunetti
• Support type: Scholarships abroad - Research Internship - Post-doctor
• FAPESP's process: 12/10000-5 - A multi-disciplinary approach to the study of amphibian diversification
• Grantee: Taran Grant
• Support type: Research Grants - Young Investigators Grants
• FAPESP's process: 17/26162-8 - Diversity and conservation of Brazilian amphibians
• Grantee: Mariana Lúcio Lyra
• Support type: Scholarships in Brazil - Technical Training Program - Technical Training
• FAPESP's process: 14/20915-6 - Chemical ecology in anurans: characterization of volatile compounds and peptide pheromones from the skin secretions of frogs
• Grantee: Andrés Eduardo Brunetti
• Support type: Scholarships in Brazil - Post-Doctorate
• FAPESP's process: 18/15425-0 - A multi-disciplinary approach to the study of amphibian diversification: phase 2
• Grantee: Taran Grant
• Support type: Research Grants - Young Investigators Grants - Phase 2
• FAPESP's process: 14/50342-8 - Amphibians of Lagamar Mosaic protected areas: diversity, conservation and perspectives
• Grantee: Célio Fernando Baptista Haddad
• Support type: Research Grants - Research Partnership for Technological Innovation - PITE