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Drastic Neofunctionalization Associated with Evolution of the Timezyme AANAT 500 Mya

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Drastic Neofunctionalization Associated with Evolution of the Timezyme AANAT 500 Mya Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya Jack Falcóna,b, Steven L. Coonc, Laurence Besseaua,b, Damien Cazaméa-Catalana,b, Michaël Fuentèsa,b, Elodie Magnanoua,b, Charles-Hubert Paulina,b, Gilles Boeufa,b,d, Sandrine Sauzeta,b,1, Even H. Jørgensene, Sylvie Mazanf, Yuri I. Wolfg, Eugene V. Kooning, Peter J. Steinbachh, Susumu Hyodoi, and David C. Kleinc,2 aCentre National de la Recherche Scientifique, Unité Mixte de Recherche 7232 and bUniversité Pierre et Marie Curie-Paris 6, Laboratoire Aragó, F-66650 Banyuls-sur-Mer, France; cSection on Neuroendocrinology, Program on Developmental Endocrinology and Genetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, gNational Center for Biotechnology Information, National Library of Medicine, and hCenter for Molecular Modeling, Center for Information Technology, National Institutes of Health, Bethesda, MD 20892; dOffice of the President, Museum National d’Histoire Naturelle, F-75005 Paris, France; eDepartment of Arctic and Marine Biology, University of Tromsø - The Arctic University of Norway, N-9037 Tromsø, Norway; fCentre National de la Recherche Scientifique, Unité Mixte de Recherche 7150, Station Biologique de Roscoff, F-29680 Roscoff, France; and iAtmosphere and Ocean Research Institute, University of Tokyo, Chiba 277-8564, Japan Edited* by Walter J. Gehring, University of Basel, Basel, Switzerland, and approved November 4, 2013 (received for review July 3, 2013) Melatonin (N-acetyl-5-methoxytrypamine) is the vertebrate hor- found in Gram-positive bacteria, protists, fungi, some lower mone of the night: circulating levels at night are markedly higher plants, algae, and cephalochordates. The broad detoxification than day levels. This increase is driven by precisely regulated role of NV-AANAT contrasts with the dedicated role that VT- increases in acetylation of serotonin in the pineal gland by arylal- AANAT plays in melatonin synthesis, which was seen in teleosts kylamine N-acetyltransferase (AANAT), the penultimate enzyme in and tetrapods (6, 18). the synthesis of melatonin. This unique essential role of AANAT in Melatonin is recognized as the vertebrate hormone of the vertebrate timekeeping is recognized by the moniker the time- night, because circulating levels are markedly elevated at night. zyme. AANAT is also found in the retina, where melatonin is In bony fish and tetrapods, VT-AANAT is highly expressed in thought to play a paracrine role. Here, we focused on the evolu- the pineal gland, the primary source of circulating melatonin (6, tion of AANAT in early vertebrates. AANATs from Agnathans (lam- 18). The unique and essential role that VT-AANAT plays in EVOLUTION prey) and Chondrichthyes (catshark and elephant shark) were vertebrate timekeeping is recognized by the moniker the time- cloned, and it was found that pineal glands and retinas from these zyme (10). VT-AANAT is also found in the retina, where N- groups express a form of AANAT that is compositionally, biochemi- acetylserotonin and/or melatonin may play paracrine roles (19). cally, and kinetically similar to AANATs found in bony vertebrates The AANAT hypothesis of pineal evolution holds that (VT-AANAT). Examination of the available genomes indicates that AANAT originally served a detoxification function in an ancestral VT-AANAT is absent from other forms of life, including the Ceph- photodetector and that its function evolved from broad acetylation alochordate amphioxus. Phylogenetic analysis and evolutionary rate estimation indicate that VT-AANAT evolved from the nonver- Significance tebrate form of AANAT after the Cephalochordate–Vertebrate split VT-AANAT over one-half billion years ago. The emergence of appar- The pineal gland is dedicated to the production of melatonin. ently involved a dramatic acceleration of evolution that accompa- Submammalian pineal glands can also detect light, and the nied neofunctionalization after a duplication of the nonvertebrate retinas of many species can make melatonin. From this finding AANAT gene. This scenario is consistent with the hypotheses that and others, it is seems that both tissues evolved from a com- VT-AANAT the advent of contributed to the evolution of the pineal mon ancestral photodetector. A key factor driving their inde- gland and lateral eyes from a common ancestral photodetector and pendent evolution may have been the evolution of melatonin that it was not a posthoc recruitment. synthesis and more specifically, the timezyme, a form of aryl- alkylamine N-acetyltransferase (AANAT) that plays a key role in yes have evolved in all animals to facilitate interactions with controlling rhythmic production of melatonin. The current re- Ethe photic environment (1, 2). However, among animals, port indicates that the timezyme evolved from a primitive form vertebrates are unique in that they also possess a photoneuro- of AANAT over 500 Mya in chordate evolution through a pro- endocrine structure, the pineal gland (3). It converts the 24-h cess of gene duplication followed by rapid neofunction- rhythm in environmental lighting into a 24-h rhythm in circu- alization and that it was not a posthoc acquisition. lating melatonin, thereby providing a unique and valuable signal of the photic environment. The details of pineal evolution are Author contributions: J.F., S.L.C., G.B., and D.C.K. designed research; S.L.C., L.B., D.C.-C., M.F., not clear (4, 5). However, it has been posited that an essential C.-H.P., S.S., E.H.J., S.M., and S.H. performed research; S.M. contributed new reagents/analytic N tools; J.F., E.M., Y.I.W., E.V.K., P.J.S., and S.H. analyzed data; J.F., S.L.C., E.V.K., and D.C.K. element was arylalkylamine -acetyltransferase (AANAT; E.C. wrote the paper; and M.F., E.J.H., and S.H. provided animal materials. 2.3.1.87), the penultimate enzyme in the melatonin biosynthesis The authors declare no conflict of interest. pathway (6–8); this scenario is referred to as the AANAT hy- pothesis of pineal evolution (7, 8). *This Direct Submission article had a prearranged editor. AANAT catalyzes the N-acetylation of arylalkylamines using Data deposition: The sequences reported in this paper have been deposited in the Gen- Bank database, www.ncbi.nlm.nih.gov/genbank/ (accession nos. EU378921, KF246473– acetyl CoA (AcCoA) as the acetyl group donor. The AANAT KF246476, KF290562, BK008791, and BK008792). family, which belongs to the GCN5 superfamily (9, 10), is com- 1Present address: Université de Lyon 1 and Centre National de la Recherche Scientifique, posed of two subfamilies termed vertebrate (VT) AANAT and † Unité Mixte de Recherche 5558, Laboratoire de Biometrie et Biologie Evolutive, F-69622 nonvertebrate (NV) AANAT. This nomenclature reflects the Villeurbanne, France. – phylogenetic distribution of the family members (13 17). The 2To whom correspondence should be addressed. E-mail: [email protected]. most striking differences between VT- and NV-AANAT are This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. found in regulatory and catalytic regions of the encoded proteins 1073/pnas.1312634110/-/DCSupplemental. (Fig. 1), consistent with different metabolic roles (7, 8). † fi The AANAT family that is the subject of the current report is distinct from another family The NV-AANAT is thought to perform a detoxi cation also named AANAT, which includes enzymes involved in acetylation of dopamine and other function through acetylation of a broad range of endogenous and arylalkylamines in insects (11, 12). These two protein families are only distantly related to exogenous arylalkylamines and polyamines (13–16). It has been each other, although both belong to the GCN5 superfamily of acetyltransferases. www.pnas.org/cgi/doi/10.1073/pnas.1312634110 PNAS Early Edition | 1of6 Downloaded by guest on September 28, 2021 Bacteria other tetrapod AANATs, with 60–73% sequence identity to Fungi other VT-AANATs. The sequence of the cloned sea lamprey Petromyzon marinus VT- Green algae AANAT (GenBank accession no. KF246473) is ∼50% identical to Amphioxus Chondrichthyes, teleost, and mammalian AANAT sequences (SI Appendix,Fig.S1), and also, it has two nonhomologous sequen- Lamprey ces: one (63 aa) at the N terminus and a second (62 aa) in the Vertebrates catalytic core. Similar nonhomologous sequences were also found in the river lamprey Lampetra fluviatilis VT-AANAT (GenBank Loop 1 Loop 2 HisƟdines Loop 3 accession no. KF290562). A truncated sequence, lacking the C-terminal end of the skate VT-AANAT, was also identified N-terminal CatalyƟc core C-terminal regulatory regulatory from the skate genome and transcriptome databases; this 163-aa region region sequence displayed 87% identity with the corresponding catshark VT-AANAT sequence (SI Appendix,Fig.S1). The organization Arylalkylamine binding Ac-CoA binding and the defining sequence features of selected AANATs are Lysine PKA/14-3-3 site CPL sequence AddiƟonal sequence summarized in Fig. 1. In addition to sequence conservation, the lamprey and other vertebrate VT-AANAT genes exhibit identical Fig. 1. Schematic organization of VT- and NV-AANATs. Major structural intron/exon structure. differences between NV- and VT-AANAT include the addition of PKA/14-3-3 Structural similarity of C. milii VT-AANAT to VT-AANATs binding sites flanking the core of the enzyme, which mediate regulation, the was also supported by modeling, in which the ovine AANAT addition of histidines to facilitate catalysis by promoting removal of protons crystal structure was used as the template. Of 166 residues generated during the transfer of the acetyl group, and the addition of a C. milii fl modeled in VT-AANAT, 107 residues (64%) are nearest short peptide sequence (Cys-Pro-Leu), which creates a oppy loop that facil- to an identical residue in the ovine template (SI Appendix, itates arylalkylamine binding and product release in the active site. The highly conserved lysine found in the N-terminal flanking regions of VT-AANAT is Fig. S2). Biochemical analysis.
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