Blastocystis is the most prevalent microbial eukaryote in the human and animal gut, yet its role as commensal or parasite is still under debate. Blastocystis has clearly undergone evolutionary adaptation to the gut environment and possesses minimal cellular compartmentalization, reduced anaerobic mitochondria, no flagella, and no reported peroxisomes. To address this poorly understood evolutionary transition, we have taken a multi-disciplinary approach to characterize Proteromonas lacertae, the closest canonical stramenopile relative of Blastocystis. Genomic data reveal an abundance of unique genes in P. lacertae but also reductive evolution of the genomic complement in Blastocystis. Comparative genomic analysis sheds light on flagellar evolution, including 37 new candidate components implicated with mastigonemes, the stramenopile morphological hallmark. The P. lacertae membrane-trafficking system (MTS) complement is only slightly more canonical than that of Blastocystis, but notably, we identified that both organisms encode the complete enigmatic endocytic TSET complex, a first for the entire stramenopile lineage. Investigation also details the modulation of mitochondrial composition and metabolism in both P. lacertae and Blastocystis. Unexpectedly, we identify in P. lacertae the most reduced peroxisome-derived organelle reported to date, which leads us to speculate on a mechanism of constraint guiding the dynamics of peroxisome-mitochondrion reductive evolution on the path to anaerobiosis. Overall, these analyses provide a launching point to investigate organellar evolution and reveal in detail the evolutionary path that Blastocystis has taken from a canonical flagellated protist to the hyper-divergent and hyper-prevalent animal and human gut microbe.

Department of Chemistry Bioscience and Environmental Engineering University of Stavanger Richard Johnsens Gate 4 4021 Stavanger Norway; Biosciences University of Exeter Stocker Road Exeter EX4 4QD UK

Department of Infection Biology Faculty of Infectious and Tropical Diseases London School of Hygiene and Tropical Medicine Keppel Street London WC1E 7HT UK

Department of Parasitology Faculty of Science Charles University BIOCEV Průmyslová 595 Vestec 252 50 Czech Republic

Division of Infectious Diseases Department of Medicine University of Alberta 1 124 Clinical Sciences Building 11350 83 Avenue Edmonton T6G 2G3 Canada; Department of Agricultural Food and Nutritional Science Faculty of Agricultural Life and Environmental Sciences University of Alberta 2 31 General Services Building Edmonton AB T6G 2H1 Canada

Division of Infectious Diseases Department of Medicine University of Alberta 1 124 Clinical Sciences Building 11350 83 Avenue Edmonton T6G 2G3 Canada; Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 1160 31 České Budějovice 370 05 Czech Republic; Centre for Life's Origin and Evolution Division of Biosciences University College London Darwin Building Gower Street London WC1E 6BT UK

Division of Infectious Diseases Department of Medicine University of Alberta 1 124 Clinical Sciences Building 11350 83 Avenue Edmonton T6G 2G3 Canada; Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 1160 31 České Budějovice 370 05 Czech Republic; Department of Parasitology Faculty of Science Charles University BIOCEV Průmyslová 595 Vestec 252 50 Czech Republic; Life Science Research Centre Department of Biology and Ecology Faculty of Science University of Ostrava Chittussiho 10 Ostrava 710 00 Czech Republic

Division of Infectious Diseases Department of Medicine University of Alberta 1 124 Clinical Sciences Building 11350 83 Avenue Edmonton T6G 2G3 Canada; School of Science Mae Fah Luang Universit 333 Moo 1 T Tasud Muang District Chiang Rai 57100 Thailand

Institute of Infection Veterinary and Ecological Sciences University of Liverpool Liverpool UK

Institute of Infection Veterinary and Ecological Sciences University of Liverpool Liverpool UK; The Earlham Institute Norwich Research Park Norwich NR4 7UZ UK

Laboratory of Molecular and Evolutionary Parasitology RAPID Group School of Biosciences University of Kent Giles Lane Stacey Building Canterbury Kent CT2 7NJ UK

Laboratory of Molecular and Evolutionary Parasitology RAPID Group School of Biosciences University of Kent Giles Lane Stacey Building Canterbury Kent CT2 7NJ UK; School of Applied Sciences Sighthill Campus Room 3 B 36 Edinburgh EH11 4BN Scotland

School of Applied Sciences Sighthill Campus Room 3 B 36 Edinburgh EH11 4BN Scotland; Faculty of Biology AG Eukaryotische Mikrobiologie Universitätsstrasse 5 S05 R04 H83 Essen 45141 Germany

School of Science Mae Fah Luang Universit 333 Moo 1 T Tasud Muang District Chiang Rai 57100 Thailand; Gut Microbiome Research Group Mae Fah Luang University 333 Moo 1 T Tasud Muang District Chiang Rai 57100 Thailand

Citace poskytuje Crossref.org

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