Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis

Autor: Dayana E. Salas-Leiva, C. Graham Clark, Martin Kolisko, Frédérique Hilliou, Mark van der Giezen, Courtney W. Stairs, Hiroshi Suga, Bernard Henrissat, Andrew J. Roger, Vladimír Klimeš, Anastasios D. Tsaousis, John M. Archibald, Steven G. Ball, Eleni Gentekaki, Richard A. Rachubinski, Darren M. Soanes, Emily K. Herman, Mary J. Klute, Marek Eliáš, Alexander Schlacht, Joel B. Dacks, Shehre-Banoo Malik, Bruce A. Curtis, Arthur W. Pightling, Maria Cecilia Arias, Laura Eme
Přispěvatelé: Faculty of Computer Science, Dalhousie University [Halifax], Architecture et fonction des macromolécules biologiques (AFMB), Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Unité de Glycobiologie Structurale et Fonctionnelle UMR 8576 (UGSF), Institut National de la Recherche Agronomique (INRA)-Université de Lille-Centre National de la Recherche Scientifique (CNRS), Department of Cell Biology [Alberta], Univerity of Alberta, 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 Science [JSPS KAKENHI 16K07468], Canadian Institutes of Health Research [FDN-143289], NSERC [RES0021028], Canadian Institutes for Health Research [MOP 142349], Gentekaki, Eleni, Roger, Andrew J., Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Unité de Glycobiologie Structurale et Fonctionnelle - UMR 8576 (UGSF), Université de Lille-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), CNRS, Université de Lille, Faculty of Sciences (Ostrava, Czech Republic), University of Alberta, Unité de Glycobiologie Structurale et Fonctionnelle - UMR 8576 [UGSF], Architecture et fonction des macromolécules biologiques [AFMB], Institut Sophia Agrobiotech [ISA], Hiroshima University, University of Exeter, Canadian Institute for Advanced Research [CIFAR], Unité de Glycobiologie Structurale et Fonctionnelle UMR 8576 [UGSF], London School of Hygiene and Tropical Medicine [LSHTM], Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Université de Lille-Centre National de la Recherche Scientifique (CNRS)
Rok vydání: 2017
Předmět:
0301 basic medicine
[SDV.BIO]Life Sciences [q-bio]/Biotechnology
MESH: Introns
MESH: Carbohydrate Metabolism
[SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology
MESH: Codon
Terminator

Biochemistry
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity
Genome
Database and Informatics Methods
Sequence alignment
[SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases
Biology (General)
Energy-Producing Organelles
Protozoans
Genetics
[SDV.MHEP.ME]Life Sciences [q-bio]/Human health and pathology/Emerging diseases
[SDV.BBM.BS]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Structural Biology [q-bio.BM]

biology
General Neuroscience
Methods and Resources
Biochemistry and Molecular Biology
Eukaryota
Genomics
Proteases
MESH: Genome
Protozoan

Vitamin biosynthesis
[SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM]
Enzymes
[SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Biomolecules [q-bio.BM]

Mitochondria
[SDV.BBM.BS]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Biomolecules [q-bio.BM]

[SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology
Proteome
Codon
Terminator

Carbohydrate Metabolism
Cellular Structures and Organelles
General Agricultural and Biological Sciences
Sequence Analysis
MESH: Blastocystis
QH301-705.5
Bioinformatics
030106 microbiology
Bioenergetics
Genome Complexity
Research and Analysis Methods
MESH: Gastrointestinal Microbiome
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
Species Specificity
Humans
MESH: Species Specificity
Gene family
[SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Biochemistry [q-bio.BM]

Gene
Comparative genomics
blastocystis
introns
comparative genomics
eukaryota
mitochondria
genomic databases
sequence alignment
Blastocystis
MESH: Humans
General Immunology and Microbiology
Organisms
Biology and Life Sciences
Computational Biology
Proteins
Cell Biology
Genome Analysis
biology.organism_classification
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
Parasitic Protozoans
Introns
Gastrointestinal Microbiome
Biological Databases
030104 developmental biology
Enzymology
[SDV.SP.PHARMA]Life Sciences [q-bio]/Pharmaceutical sciences/Pharmacology
Genome
Protozoan

Genomic databases
Biokemi och molekylärbiologi
Zdroj: PLoS Biology
PLoS Biology, Public Library of Science, 2017, 15 (9), pp.e2003769. ⟨10.1371/journal.pbio.2003769⟩
Plos Biology 9 (15), . (2017)
PLoS Biology, 2017, 15 (9), pp.e2003769. ⟨10.1371/journal.pbio.2003769⟩
PLoS Biology, Vol 15, Iss 9, p e2003769 (2017)
ISSN: 1545-7885
1544-9173
Popis: 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.
Author summary Blastocystis are unicellular eukaryotic organisms related to algae and some plant pathogens. They are common constituents of the human gut microbial community, colonizing approximately 1 billion humans worldwide. Whether their presence is harmful or not continues to be hotly debated. Part of the uncertainty stems from the fact that at least 17 subtypes have been identified from various mammalian hosts, including 9 from humans. To better characterize and understand Blastocystis, we have sequenced and annotated the genome for subtype 1 and compared it with previous genomic results for subtypes 7 and 4. The comparisons revealed considerable differences between the 3 sequenced subtypes for a number of genomic features like DNA base composition, size of genome, number of genes, and number of introns. We also examined various biochemical pathways and cellular systems in the context of the full gene complement to better understand the biology of Blastocystis, including some of its more unusual features like a mitochondrion related organelle. We also identified subtype-specific gene family expansions that may be related to virulence. Finally, we showed that Blastocystis appears to have most of the genes necessary for sexual reproduction. This study provides resources and hypotheses for future investigations into the biology and potential pathogenicity of these common gut microbes.
Databáze: OpenAIRE