Reconstructing the Mosaic Glycolytic Pathway of the Anaerobic Eukaryote Monocercomonoides

Abstract

All eukaryotes carry out glycolysis, interestingly, not all using the same enzymes. Anaerobic eukaryotes face the challenge of fewer molecules of ATP extracted per molecule of glucose due to their lack of a complete tricarboxylic acid cycle. This may have pressured anaerobic eukaryotes to acquire the more ATP-efficient alternative glycolytic enzymes, such as pyrophosphate-fructose 6-phosphate phosphotransferase and pyruvate orthophosphate dikinase, through lateral gene transfers from bacteria and other eukaryotes. Most studies of these enzymes in eukaryotes involve pathogenic anaerobes; Monocercomonoides, an oxymonad belonging to the eukaryotic supergroup Excavata, is a nonpathogenic anaerobe representing an evolutionarily and ecologically distinct sampling of an anaerobic glycolytic pathway. We sequenced cDNA encoding glycolytic enzymes from a previously established cDNA library of Monocercomonoides and analyzed the relationships of these enzymes to those from other organisms spanning the major groups of Eukaryota, Bacteria, and Archaea. We established that, firstly, Monocercomonoides possesses alternative versions of glycolytic enzymes: fructose-6-phosphate phosphotransferase, both pyruvate kinase and pyruvate orthophosphate dikinase, cofactor-independent phosphoglycerate mutase, and fructose-bisphosphate aldolase (class II, type B). Secondly, we found evidence for the monophyly of oxymonads, kinetoplastids, diplomonads, and parabasalids, the major representatives of the Excavata. We also found several prokaryote-to-eukaryote as well as eukaryote-to-eukaryote lateral gene transfers involving glycolytic enzymes from anaerobic eukaryotes, further suggesting that lateral gene transfer was an important factor in the evolution of this pathway for denizens of this environment.

Estrogen‐responsive nitroso‐proteome in uterine artery endothelial cells: Role of endothelial nitric oxide synthase and estrogen receptor‐β

“…Aldehyde reductase is primarily known for catalyzing the reduction of glucose to sorbitol, the first step in polyol pathway of glucose metabolism (Petrash, 2004). Pyruvate kinase is an enzyme also involved in glycolysis (Liapounova et al, 2006). Citrate synthase exists in nearly all living cells and stands as a pace-making enzyme in the first step of the citric acid cycle (Wiegand and Remington, 1986).…”

Molecular paleontology and complexity in the last eukaryotic common ancestor

“…Thiergart et al ., 2012). However, several major pathways, such as glycolysis, have probably experienced significant HGT and gene displacement post-LECA, most notably during the evolution of anaerobic/microaerophilic lineages (Liapounova et al ., 2006; Stechmann et al ., 2006). Thus catabolism of glucose, the carbon source for ATP production preferred by the majority of extant eukaryotes, is catalyzed by orthologs of classic Embden-Meyerhof glycolytic enzymes, and not the variants present in some archaea (Sato & Atomi, 2011; Siebers & Schönheit, 2005).…”

Intermediary Metabolism in Protists: a Sequence-based View of Facultative Anaerobic Metabolism in Evolutionarily Diverse Eukaryotes

“…However, just as LGT facilitates innovation of novel metabolic traits, it can also facilitate gene displacement. Mosaic origins of some glycolytic enzymes in anaerobic protists provide good examples of displacement (Liapounova et al 2006; Stechmann et al 2006). Differences in V max , substrate affinities, etc, which conceivably effect changes in metabolic flux along a pathway such as glycolysis provide the obvious selective advantages that could result in the retention of a gene encoding a laterally transferred enzyme within a recipient genome, followed by an eventual displacement and loss of the ancestral endogenous gene that encoded the original isoform.…”