Evolutionary analysis of cellular reduction and anaerobicity in the hyper-prevalent gut microbe Blastocystis

0574496 - BC 2024 RIV US eng J - Journal Article
Záhonová, Kristýna - Low, R. S. - Warren, C.J. - Cantoni, D. - Herman, E.K. - Yiangou, L. - Ribeiro, C.A. - Phanprasert, Y. - Brown, I.R. - Rueckert, S. - Baker, N.L. - Tachezy, J. - Betts, E.L. - Gentekaki, E. - van der Giezen, M. - Clark, C.G. - Jackson, A.P. - Dacks, Joel Bryan - Tsaousis, A.D.
Evolutionary analysis of cellular reduction and anaerobicity in the hyper-prevalent gut microbe Blastocystis.
Current Biology. Roč. 33, č. 12 (2023), s. 2449-+. ISSN 0960-9822. E-ISSN 1879-0445
Institutional support: RVO:60077344
Keywords : peroxisome * comparative genomics * flagella
OECD category: Biochemistry and molecular biology
Impact factor: 9.2, year: 2022
Method of publishing: Open access
https://www.sciencedirect.com/science/article/pii/S0960982223006206?via%3Dihub

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 multidisciplinary 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.
Permanent Link: https://hdl.handle.net/11104/0345307