title: Lateral Gene Transfer in the Adaptation of the Anaerobic Parasite Blastocystis to the Gut.
abstract: Blastocystis spp. are the most prevalent eukaryotic microbes found in the intestinal tract of humans. Here we present an in-depth investigation of lateral gene transfer (LGT) in the genome of Blastocystis sp. subtype 1. Using rigorous phylogeny-based methods and strict validation criteria, we show that ∼2.5% of the genes of this organism were recently acquired by LGT. We identify LGTs both from prokaryote and eukaryote donors. Several transfers occurred specifically in ancestors of a subset of Blastocystis subtypes, demonstrating that LGT is an ongoing process. Functional predictions reveal that these genes are involved in diverse metabolic pathways, many of which appear related to adaptation of Blastocystis to the gut environment. Specifically, we identify genes involved in carbohydrate scavenging and metabolism, anaerobic amino acid and nitrogen metabolism, oxygen-stress resistance, and pH homeostasis. A number of the transferred genes encoded secreted proteins that are potentially involved in infection, escaping host defense, or most likely affect the prokaryotic microbiome and the inflammation state of the gut. We also show that Blastocystis subtypes differ in the nature and copy number of LGTs that could relate to variation in their prevalence and virulence. Finally, we identified bacterial-derived genes encoding NH3-dependent nicotinamide adenine dinucleotide (NAD) synthase in Blastocystis and other protozoan parasites, which are promising targets for drug development. Collectively, our results suggest new avenues for research into the role of Blastocystis in intestinal disease and unequivocally demonstrate that LGT is an important mechanism by which eukaryotic microbes adapt to new environments.
authors.affiliation: Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College Street, Halifax, NS B3H 4R2, Canada.
authors.forename: Laura
authors.initials: L
authors.lastname: Eme
authors.affiliation: School of Science and Human Gut Microbiome for Health Research Unit, Mae Fah Luang University, Chiang Rai 57100, Thailand.
authors.forename: Eleni
authors.initials: E
authors.lastname: Gentekaki
authors.affiliation: Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College Street, Halifax, NS B3H 4R2, Canada.
authors.forename: Bruce
authors.initials: B
authors.lastname: Curtis
authors.affiliation: Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College Street, Halifax, NS B3H 4R2, Canada; Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, 180 Dundas Street W., Toronto, ON M5G 1Z8, Canada.
authors.forename: John M
authors.initials: JM
authors.lastname: Archibald
authors.affiliation: Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College Street, Halifax, NS B3H 4R2, Canada; Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, 180 Dundas Street W., Toronto, ON M5G 1Z8, Canada. Electronic address: andrew.roger@dal.ca.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Roger
mesh_terms: D000064:Acclimatization; D016844:Blastocystis / Q000235:genetics / Q000502:physiology*; D016776:Blastocystis Infections / Q000469:parasitology*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D006801:Humans; D007410:Intestinal Diseases / Q000469:parasitology*; D007422:Intestines / Q000469:parasitology*; D064307:Microbiota
keywords: Blastocystis; Crohn’s disease; NAD synthase; adaptation; anaerobiosis; immune evasion; lateral gene transfer; parasite; pathogenicity; protist