Reconstructing the mosaic glycolytic pathway of the anaerobic eukaryote Monocercomonoides.
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.
Liapounova
Natalia A
NA
Department of Biological Sciences, the University of Calgary, Calgary, Alberta T2N 1N4, Canada.
Hampl
Vladimir
V
Gordon
Paul M K
PM
Sensen
Christoph W
CW
Gedamu
Lashitew
L
Dacks
Joel B
JB
D000693:Anaerobiosis; D000818:Animals; D056890:Eukaryota / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D005057:Eukaryotic Cells; D019143:Evolution, Molecular; D006019:Glycolysis / Q000235:genetics / Q000502:physiology; D006593:Hexokinase / Q000235:genetics / Q000378:metabolism; D008969:Molecular Sequence Data; D025221:Phosphofructokinases / Q000235:genetics / Q000378:metabolism; D010736:Phosphoglycerate Mutase / Q000235:genetics / Q000378:metabolism; D010751:Phosphopyruvate Hydratase / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny
D025221:Phosphofructokinases; D006593:Hexokinase; D010751:Phosphopyruvate Hydratase; D010736:Phosphoglycerate Mutase