Abstract

Glycolysis is a central metabolic pathway in eukaryotic and prokaryotic cells. In eukaryotes, the textbook view is that glycolysis occurs in the cytosol. However, fusion proteins comprised of two glycolytic enzymes, triosephosphate isomerase (TPI) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH), were found in members of the stramenopiles (diatoms and oomycetes) and shown to possess amino-terminal mitochondrial targeting signals. Here we show that mitochondrial TPI-GAPDH fusion protein genes are widely spread across the known diversity of stramenopiles, including non-photosynthetic species (Bicosoeca sp. and Blastocystis hominis). We also show that TPI-GAPDH fusion genes exist in three cercozoan taxa (Paulinella chromatophora, Thaumatomastix sp. and Mataza hastifera) and an apusozoan protist, Thecamonas trahens. Interestingly, subcellular localization predictions for other glycolytic enzymes in stramenopiles and a cercozoan show that a significant fraction of the glycolytic enzymes in these species have mitochondrial-targeted isoforms. These results suggest that part of the glycolytic pathway occurs inside mitochondria in these organisms, broadening our knowledge of the diversity of mitochondrial metabolism of protists.

Highlights

  • Glycolysis is a fundamental catabolic biochemical pathway occurring in essentially all living cells

  • We have shown that triosephosphate isomerase (TPI)-glyceraldehyde-3-phosphate dehydrogenase (GAPDH) fusion proteins exist in Bicosoeca sp. and Blastocystis hominis, two ‘basal’ stramenopiles [15], as well as in heterokontophytes and oomycetes, implying a broad distribution within stramenopiles

  • The TPI-GAPDH fusion protein genes were found in cercozoan species belonging to the ‘supergroup’ Rhizaria, as well as the apusozoan Thecamonas trahens whose exact phylogenetic position among eukaryotes is not known [40]

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Summary

Introduction

Glycolysis is a fundamental catabolic biochemical pathway occurring in essentially all living cells. The sequential reactions of the glycolytic pathway generally occur in the cytosol and the end product, pyruvate, is transported to the mitochondrion for subsequent participation in the TCA cycle. This textbook version of eukaryotic glycolysis is based mainly on studies of plants and animals, evidence suggests that at least some unicellular eukaryotes–protists–deviate from the canonical glycolytic pathway. Atypical compartmentalization of glycolytic enzymes is seen in trypanosomatid protists (i.e., Trypanosoma spp. and Leishmania spp.), well known as the causative agents of human diseases [1,2]. Trypanosomatids possess a peroxisome-like structure called a glycosome and enzymes involved in the first part of glycolysis (from hexokinase to phosphoglycerate kinase) function in this membrane-enclosed compartment [3,4,5,6]

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