Abstract
The traditional assumption that bats cannot synthesize vitamin C (Vc) has been challenged recently. We have previously shown that two Old World bat species (Rousettus leschenaultii and Hipposideros armiger) have functional L-gulonolactone oxidase (GULO), an enzyme that catalyzes the last step of Vc biosynthesis de novo. Given the uncertainties surrounding when and how bats lost GULO function, exploration of gene evolutionary patterns is needed. We therefore sequenced GULO genes from 16 bat species in 5 families, aiming to establish their evolutionary histories. In five cases we identified pseudogenes for the first time, including two cases in the genus Pteropus (P. pumilus and P. conspicillatus) and three in family Hipposideridae (Coelops frithi, Hipposideros speoris, and H. bicolor). Evolutionary analysis shows that the Pteropus clade has the highest ω ratio and has been subjected to relaxed selection for less than 3 million years. Purifying selection acting on the pseudogenized GULO genes of roundleaf bats (family Hipposideridae) suggests they have lost the ability to synthesize Vc recently. Limited mutations in the reconstructed GULO sequence of the ancestor of all bats contrasts with the many mutations in the ancestral sequence of recently emerged Pteropus bats. We identified at least five mutational steps that were then related to clade origination times. Together, our results suggest that bats lost the ability to biosynthesize vitamin C recently by exhibiting stepwise mutation patterns during GULO evolution that can ultimately lead to pseudogenization.
Highlights
Vitamin C (Vc), or L-ascorbic acid is a water-soluble vitamin that is an essential nutrient impotant in animal metabolism
As gulonolactone oxidase (GULO) is present in all major vertebrate lineages except some bats [8], anthropoid primates [12], [26], guinea pigs [11], some passerine birds [27], and some fishes [5], such loss-of-function is neither related to broad phylogenetic affiliations nor to diet [28]
Our results show a range of forms of the GULO gene in bats
Summary
Vitamin C (Vc), or L-ascorbic acid is a water-soluble vitamin that is an essential nutrient impotant in animal metabolism. Vc is involved in tissue growth and repair, and functions as an antioxidant to block damage caused by free radicals. It is a cofactor in enzymatic reactions that are catalyzed by Cu+dependent monooxygenases and Fe2+-dependent dioxygenases [1]. Vc is required in the diet of all vertebrates in order to sustain good health [2], and Vc deficiency can lead to potentially fatal scurvy in humans. Most vertebrates can satisfy their Vc requirements by synthesizing it de novo with glucose [3]. The ability to synthesize Vc has been reported in many ancestral vertebrate lineages [5], [6], suggesting the ability for de novo synthesis is ancient. There is an apparent transition of the organs used for the biosynthesis of Vc during evolution, from the kidney of reptiles to the liver of mammals [7]
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