title: Decay of the glycolytic pathway and adaptation to intranuclear parasitism within Enterocytozoonidae microsporidia.
abstract: Glycolysis and oxidative phosphorylation are the fundamental pathways of ATP generation in eukaryotes. Yet in microsporidia, endoparasitic fungi living at the limits of cellular streamlining, oxidative phosphorylation has been lost: energy is obtained directly from the host or, during the dispersive spore stage, via glycolysis. It was therefore surprising when the first sequenced genome from the Enterocytozoonidae - a major family of human and animal-infecting microsporidians - appeared to have lost genes for glycolysis. Here, we sequence and analyse genomes from additional members of this family, shedding new light on their unusual biology. Our survey includes the genome of Enterocytozoon hepatopenaei, a major aquacultural parasite currently causing substantial economic losses in shrimp farming, and Enterospora canceri, a pathogen that lives exclusively inside epithelial cell nuclei of its crab host. Our analysis of gene content across the clade suggests that Ent. canceri's adaptation to intranuclear life is underpinned by the expansion of transporter families. We demonstrate that this entire lineage of pathogens has lost glycolysis and, uniquely amongst eukaryotes, lacks any obvious intrinsic means of generating energy. Our study provides an important resource for the investigation of host-pathogen interactions and reductive evolution in one of the most medically and economically important microsporidian lineages.
authors.affiliation: Biosciences, College of Life and Environmental Sciences, University of Exeter, EX4 4QD, UK.
authors.forename: Dominic
authors.initials: D
authors.lastname: Wiredu Boakye
authors.affiliation: Department of Biochemistry, Faculty of Science, Mahidol University, Rama VI Rd, Bangkok, 10400, Thailand.|Center of Excellence for Shrimp Molecular Biology and Biotechnology, Faculty of Science, Mahidol University, Rama VI Rd, Bangkok, 10400, Thailand.
authors.forename: Pattana
authors.initials: P
authors.lastname: Jaroenlak
authors.affiliation: Shrimp-Virus Interaction Laboratory (ASVI), National Center for Genetic Engineering and Biotechnology (BIOTEC), Rama VI Rd, Bangkok, 10400, Thailand.
authors.forename: Anuphap
authors.initials: A
authors.lastname: Prachumwat
authors.affiliation: School of Earth Sciences, University of Bristol, BS8 1TH, UK.
authors.forename: Tom A
authors.initials: TA
authors.lastname: Williams
authors.affiliation: European Union Reference Laboratory for Crustacean Diseases, Centre for Environment Fisheries and Aquaculture Science, Weymouth Laboratory, Weymouth, Dorset, DT4 8UB, UK.
authors.forename: Kelly S
authors.initials: KS
authors.lastname: Bateman
authors.affiliation: Department of Biochemistry, Faculty of Science, Mahidol University, Rama VI Rd, Bangkok, 10400, Thailand.|Center of Excellence for Shrimp Molecular Biology and Biotechnology, Faculty of Science, Mahidol University, Rama VI Rd, Bangkok, 10400, Thailand.
authors.forename: Ornchuma
authors.initials: O
authors.lastname: Itsathitphaisarn
authors.affiliation: Shrimp-Virus Interaction Laboratory (ASVI), National Center for Genetic Engineering and Biotechnology (BIOTEC), Rama VI Rd, Bangkok, 10400, Thailand.
authors.forename: Kallaya
authors.initials: K
authors.lastname: Sritunyalucksana
authors.affiliation: Biosciences, College of Life and Environmental Sciences, University of Exeter, EX4 4QD, UK.
authors.forename: Konrad H
authors.initials: KH
authors.lastname: Paszkiewicz
authors.affiliation: Biosciences, College of Life and Environmental Sciences, University of Exeter, EX4 4QD, UK.
authors.forename: Karen A
authors.initials: KA
authors.lastname: Moore
authors.affiliation: European Union Reference Laboratory for Crustacean Diseases, Centre for Environment Fisheries and Aquaculture Science, Weymouth Laboratory, Weymouth, Dorset, DT4 8UB, UK.
authors.forename: Grant D
authors.initials: GD
authors.lastname: Stentiford
authors.affiliation: Biosciences, College of Life and Environmental Sciences, University of Exeter, EX4 4QD, UK.
authors.forename: Bryony A P
authors.initials: BAP
authors.lastname: Williams
mesh_terms: D000818:Animals; D001483:Base Sequence; D005075:Biological Evolution; D021862:Enterocytozoon / Q000235:genetics / Q000378:metabolism* / Q000472:pathogenicity; D018503:Genome, Protozoan / Q000235:genetics*; D006019:Glycolysis / Q000235:genetics*; D006593:Hexokinase / Q000235:genetics*; D006790:Host-Parasite Interactions / Q000502:physiology*; D006801:Humans; D016881:Microsporidiosis / Q000469:parasitology; D010085:Oxidative Phosphorylation; D033561:Penaeidae / Q000469:parasitology*; D010802:Phylogeny; D017422:Sequence Analysis, DNA
chemical_list: D006593:Hexokinase