The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism

Abstract

Reduction of various biological processes is a hallmark of the parasitic lifestyle. Generally, the more intimate the association between parasites and hosts the stronger the parasite relies on its host's physiology for survival and reproduction. However, some systems have been held to be indispensable, for example, the core pathways of carbon metabolism that produce energy from sugars. Even the most hardened anaerobes that lack oxidative phosphorylation and the tricarboxylic acid cycle have retained glycolysis and some downstream means to generate ATP. Here we describe the deep-coverage genome resequencing of the pathogenic microsporidiian, Enterocytozoon bieneusi, which shows that this parasite has crossed this line and abandoned complete pathways for the most basic carbon metabolism. Comparing two genome sequence surveys of E. bieneusi to genomic data from four other microsporidia reveals a normal complement of 353 genes representing 30 functional pathways in E. bieneusi, except that only 2 out of 21 genes collectively involved in glycolysis, pentose phosphate, and trehalose metabolism are present. Similarly, no genes encoding proteins involved in the processing of spliceosomal introns were found. Altogether, E. bieneusi appears to have no fully functional pathway to generate ATP from glucose. Therefore, this intracellular parasite relies on transporters to import ATP from its host.

FIG. 1.—

Core carbon metabolic pathways believed to form the backbone of energy metabolism in microsporidia. Enzymes are in red and metabolites in black. All the enzymes shown are present in the genomes of Encephalitozoon cuniculi, Antonospora locustae, Nosema ceranae, and Octosporea bayeri, with the single exception of lactonase (in gray) which has not been identified. In contrast, only two enzymes in any of these pathways are present in Enterocytozoon bieneusi (shown in red on black).