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Open Access Research article

Evolution of AANAT: expansion of the gene family in the cephalochordate amphioxus

Jiri Pavlicek1, Sandrine Sauzet2, Laurence Besseau2, Steven L Coon1, Joan L Weller1, Gilles Boeuf23, Pascaline Gaildrat1, Marina V Omelchenko4, Eugene V Koonin4, Jack Falcón2 and David C Klein1*

Author Affiliations

1 Section on Neuroendocrinology, Program in Developmental Endocrinology and Genetics, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, 20892, MD, USA

2 Laboratoire Arago, UPMC-Paris 6 and CNRS, FRE 3247 & GDR 2821, Facteurs du Milieu & Mécanismes Adaptatifs, Banyuls/Mer, 66651, France

3 Museum National d'Histoire Naturelle (MNHN), 43 rue Cuvier, Paris, 75005, France

4 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, 20894, MD, USA

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BMC Evolutionary Biology 2010, 10:154  doi:10.1186/1471-2148-10-154

Published: 25 May 2010

Abstract

Background

The arylalkylamine N-acetyltransferase (AANAT) family is divided into structurally distinct vertebrate and non-vertebrate groups. Expression of vertebrate AANATs is limited primarily to the pineal gland and retina, where it plays a role in controlling the circadian rhythm in melatonin synthesis. Based on the role melatonin plays in biological timing, AANAT has been given the moniker "the Timezyme". Non-vertebrate AANATs, which occur in fungi and protists, are thought to play a role in detoxification and are not known to be associated with a specific tissue.

Results

We have found that the amphioxus genome contains seven AANATs, all having non-vertebrate type features. This and the absence of AANATs from the genomes of Hemichordates and Urochordates support the view that a major transition in the evolution of the AANATs may have occurred at the onset of vertebrate evolution. Analysis of the expression pattern of the two most structurally divergent AANATs in Branchiostoma lanceolatum (bl) revealed that they are expressed early in development and also in the adult at low levels throughout the body, possibly associated with the neural tube. Expression is clearly not exclusively associated with the proposed analogs of the pineal gland and retina. blAANAT activity is influenced by environmental lighting, but light/dark differences do not persist under constant light or constant dark conditions, indicating they are not circadian in nature. bfAANATα and bfAANATδ' have unusually alkaline (> 9.0) optimal pH, more than two pH units higher than that of vertebrate AANATs.

Conclusions

The substrate selectivity profiles of bfAANATα and δ' are relatively broad, including alkylamines, arylalkylamines and diamines, in contrast to vertebrate forms, which selectively acetylate serotonin and other arylalkylamines. Based on these features, it appears that amphioxus AANATs could play several roles, including detoxification and biogenic amine inactivation. The presence of seven AANATs in amphioxus genome supports the view that arylalkylamine and polyamine acetylation is important to the biology of this organism and that these genes evolved in response to specific pressures related to requirements for amine acetylation.