Journal Article

Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis

Roger, Andrew, Architecture et fonction des macromolécules biologiques (AFMB) ; Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Gentekaki, Eleni, Soanes, Darren, Arias, Maria, Institut Sophia Agrobiotech (ISA) ; Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS)-Centre National de la Recherche Scientifique (CNRS), Ball, Steven, Suga, Hiroshi, Henrissat, Bernard, Unité de Glycobiologie Structurale et Fonctionnelle - UMR 8576 (UGSF) ; Université de Lille-Centre National de la Recherche Scientifique (CNRS), Department of Cell Biology [Alberta] ; University of Alberta, Clark, C Graham, Kolisko, Martin, Archibald, John, Stairs, Courtney, Klimeš, Vladimír, van Der Giezen, Mark, Biotechnology and Biological Sciences Research Council [BB/M009971/1]; Czech Science Foundation [13-33039S, 15-16406S]; Wellcome Trust [078566/A/05/Z]; Wellcome Trust; Japan Society for the Promotion of Scienc

2017

Overview

Blastocystis is the most prevalent eukaryotic microbe colonizing the human gut, infecting approximately 1 billion individuals worldwide. Although Blastocystis has been linked to intestinal disorders, its pathogenicity remains controversial because most carriers are asymptomatic. Here, the genome sequence of Blastocystis subtype (ST) 1 is presented and compared to previously published sequences for ST4 and ST7. Despite a conserved core of genes, there is unexpected diversity between these STs in terms of their genome sizes, guanine-cytosine (GC) content, intron numbers, and gene content. ST1 has 6,544 protein-coding genes, which is several hundred more than reported for ST4 and ST7. The percentage of proteins unique to each ST ranges from 6.2% to 20.5%, greatly exceeding the differences observed within parasite genera. Orthologous proteins also display extreme divergence in amino acid sequence identity between STs (i.e., 59%-61% median identity), on par with observations of the most distantly related species pairs of parasite genera. The STs also display substantial variation in gene family distributions and sizes, especially for protein kinase and protease gene families, which could reflect differences in virulence. It remains to be seen to what extent these inter-ST differences persist at the intra-ST level. A full 26% of genes in ST1 have stop codons that are created on the mRNA level by a novel polyadenylation mechanism found only in Blastocystis. Reconstructions of pathways and organellar systems revealed that ST1 has a relatively complete membrane-trafficking system and a near-complete meiotic toolkit, possibly indicating a sexual cycle. Unlike some intestinal protistan parasites, Blastocystis ST1 has near-complete de novo pyrimidine, purine, and thiamine biosynthesis pathways and is unique amongst studied stramenopiles in being able to metabolize α-glucans rather than β-glucans. It lacks all genes encoding heme-containing cytochrome P450 proteins. Predictions of the mitochondrion-related organelle (MRO) proteome reveal an expanded repertoire of functions, including lipid, cofactor, and vitamin biosynthesis, as well as proteins that may be involved in regulating mitochondrial morphology and MRO/endoplasmic reticulum (ER) interactions. In sharp contrast, genes for peroxisome-associated functions are absent, suggesting Blastocystis STs lack this organelle. Overall, this study provides an important window into the biology of Blastocystis, showcasing significant differences between STs that can guide future experimental investigations into differences in their virulence and clarifying the roles of these organisms in gut health and disease.

• Publisher: Public Library of Science,CCSD,Public Library of Science (PLoS)
• Subject: Amino acid sequence / Amino acids / Bacteriology / Biochemistry / Biochemistry, Molecular Biology / Bioinformatics / Biological diversity / Biology and Life Sciences / Biosynthesis / Biotechnology / Blastocystis / Blastocystis - genetics / Blastocystis - metabolism / Carbohydrate Metabolism / Codon, Terminator / Codons / Cytochrome / Cytochrome P450 / Cytosine / Digestive system / Digestive tract / Divergence / Emerging diseases / Endoplasmic reticulum / Environmental science / Enzymes / Gastrointestinal Microbiome / Gastrointestinal tract / Gene families / Gene sequencing / Genes / Genetic aspects / Genome, Protozoan / Genomes / Genomics / Glucans / Guanine / Heme / Human health and pathology / Humans / Immunology / Infectious diseases / Innate immunity / Intestine / Introns / Life Sciences / Meiosis / Membrane trafficking / Methods / Methods and Resources / Microbiology and Parasitology / Mitochondria / Molecular biology / mRNA / Neurobiology / Neurons and Cognition / Nucleotide sequence / Observations / Parasites / Parasitic diseases / Parasitology / Pathogenicity / Pathogens / Pharmaceutical sciences / Pharmacology / Phylogenetics / Polyadenylation / Prokaryotes / Protein kinase / Proteins / Proteomes / Quantitative Methods / Research and Analysis Methods / Software / Species Specificity / Structural Biology / Supervision / Thiamine / Virology / Virulence / β-Glucan
• ISBN: 0004119782000