Abstract
Ascorbic acid (vitamin C) is an enzyme co-factor in eukaryotes that also plays a critical role in protecting photosynthetic eukaryotes against damaging reactive oxygen species derived from the chloroplast. Many animal lineages, including primates, have become ascorbate auxotrophs due to the loss of the terminal enzyme in their biosynthetic pathway, L-gulonolactone oxidase (GULO). The alternative pathways found in land plants and Euglena use a different terminal enzyme, L-galactonolactone dehydrogenase (GLDH). The evolutionary processes leading to these differing pathways and their contribution to the cellular roles of ascorbate remain unclear. Here we present molecular and biochemical evidence demonstrating that GULO was functionally replaced with GLDH in photosynthetic eukaryote lineages following plastid acquisition. GULO has therefore been lost repeatedly throughout eukaryote evolution. The formation of the alternative biosynthetic pathways in photosynthetic eukaryotes uncoupled ascorbate synthesis from hydrogen peroxide production and likely contributed to the rise of ascorbate as a major photoprotective antioxidant.
Highlights
Ascorbate plays an essential role in eukaryotes as an enzyme co-factor in hydroxylation reactions, contributing to diverse processes such as the synthesis of collagen and the demethylation of histones and nucleic acids role in eukaryotes to help protect against reactive oxygen species (ROS) derived from metabolic activity
What is the wider distribution of gulonolactone oxidase (GULO) loss and ascorbate auxotrophy in the metazoa? 2) do all photosynthetic eukaryotes use an alternative terminal enzyme to animals? 3) why do two different pathways using galactonolactone dehydrogenase (GLDH) exist in photosynthetic eukaryotes? 4) which pathway is used in the rhodophytes? Using a combination of molecular and biochemical analyses, we present evidence that GULO is an ancestral gene in eukaryotes that has been functionally replaced by GLDH in the photosynthetic lineages, resulting in the development of their alternative biosynthetic pathways
Derived metazoans, including sponges and cnidarians, and is present in a filasterean (Capsaspora owczarzaki) and in fungi (Supplementary File 1). This suggests that ascorbate synthesis via GULO is an ancestral trait in the Opisthokonta that has been lost in many lineages
Summary
Ascorbate (vitamin C) plays an essential role in eukaryotes as an enzyme co-factor in hydroxylation reactions, contributing to diverse processes such as the synthesis of collagen and the demethylation of histones and nucleic acids role in eukaryotes to help protect against reactive oxygen species (ROS) derived from metabolic activity. The majority of hydrogen peroxide (H2O2) generated in some organelles is likely reduced by other antioxidant systems, such as the peroxiredoxins and glutathione peroxidases in the mitochondria, and catalases in the peroxisome plays a role in protecting photosynthetic cells against ROS derived from the chloroplast 5. Thylakoid- and stromalocalised APX removes H2O2 produced by photosystem I through the activity of the ascorbate-glutathione cycle and this process may account for 10% of photosynthetic electron transport flow. Ascorbate in the thylakoid lumen may prevent photoinhibition in high light by directly donating electrons to the photosynthetic electron transport chain 5. These roles have been demonstrated in a range of ascorbate deficient plants that display sensitivity to high light and to oxidants
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