Abstract
ABSTRACTNeocallimastigomycetes are unique examples of strictly anaerobic eukaryotes. This study investigates how these anaerobic fungi bypass reactions involved in synthesis of pyridine nucleotide cofactors and coenzyme A that, in canonical fungal pathways, require molecular oxygen. Analysis of Neocallimastigomycetes proteomes identified a candidate l-aspartate-decarboxylase (AdcA) and l-aspartate oxidase (NadB) and quinolinate synthase (NadA), constituting putative oxygen-independent bypasses for coenzyme A synthesis and pyridine nucleotide cofactor synthesis. The corresponding gene sequences indicated acquisition by ancient horizontal gene transfer (HGT) events involving bacterial donors. To test whether these enzymes suffice to bypass corresponding oxygen-requiring reactions, they were introduced into fms1Δ and bna2Δ Saccharomyces cerevisiae strains. Expression of nadA and nadB from Piromyces finnis and adcA from Neocallimastix californiae conferred cofactor prototrophy under aerobic and anaerobic conditions. This study simulates how HGT can drive eukaryotic adaptation to anaerobiosis and provides a basis for elimination of auxotrophic requirements in anaerobic industrial applications of yeasts and fungi.
Highlights
Neocallimastigomycetes are obligately anaerobic fungi with specialized metabolic adaptations that allow them to play a key role in the degradation of recalcitrant plant biomass in herbivore guts [1]
Identification of a candidate oxygen-independent L-aspartate decarboxylase involved in coenzyme A (CoA) synthesis in anaerobic fungi
Decarboxylation of L-aspartate to b-alanine by L-aspartate decarboxylase (Adc), an enzyme that occurs in many species across all domains of life [23], enables an oxygen-independent alternative for the canonical fungal pathway for CoA synthesis (Fig. 1)
Summary
Neocallimastigomycetes are obligately anaerobic fungi with specialized metabolic adaptations that allow them to play a key role in the degradation of recalcitrant plant biomass in herbivore guts [1]. Instead of sterols, which occur in membranes of virtually all other eukaryotes [9] and whose biosynthesis involves multiple oxygen-dependent reactions [10], Neocallimastigomycetes contain tetrahymanol [3, 6]. The Neocallimastigomycetae Neocallimastix patriciarum has been shown to grow in synthetic media lacking precursors for pyridine nucleotide and CoA synthesis [18] This observation indicates that at least some anaerobic fungi harbor oxygen-independent pathways for synthesizing these essential cofactors. Fungal NAD1 and Coenzyme A Oxygen-Independent Pathways requiring enzymes of the kynurenine pathway Instead, their genomes were reported to harbor genes encoding an L-aspartate oxidase (NadB) and quinolinate synthase (NadA), two enzymes active in the bacterial pathway for NAD1 synthesis [6] (Fig. 1, right). No hypothesis has yet been forwarded on how these fungi may bypass the oxygen requirement for the canonical fungal CoA biosynthesis route
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