Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis.
van der Giezen, M
Public Library of Science
© 2017 Gentekaki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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.
Biotechnology and Biological Sciences Research Council http://www.bbsrc.ac.uk/ (grant number BB/M009971/1). Received by ADT. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Czech Science Foundation https://gacr.cz/en/ (grant number 13-33039S, 15-16406S). Received by ME. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Wellcome Trust https://wellcome.ac.uk/ (grant number 078566/A/05/Z). MvdG and CGC are grateful for support from the Wellcome Trust. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Japan Society for the Promotion of Science http://www.jsps.go.jp/english/ (grant number JSPS KAKENHI 16K07468). Received by HS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Canadian Institutes of Health Research http://www.cihr-irsc.gc.ca/e/193.html (grant number FDN-143289). Received by RAR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NSERC http://www.nserc-crsng.gc.ca/index_eng.asp (grant number RES0021028). Received by JBD. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Canadian Institutes for Health Research http://www.cihr-i9rsc.gc.ca/e/193.html (grant number MOP-142349). Received by AJR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Vol. 15, e2003769
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