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

• Published in: Current biology Vol. 33; no. 12; pp. 2449 - 2464.e8
• Main Authors: Záhonová, Kristína, Low, Ross S., Warren, Christopher J., Cantoni, Diego, Herman, Emily K., Yiangou, Lyto, Ribeiro, Cláudia A., Phanprasert, Yasinee, Brown, Ian R., Rueckert, Sonja, Baker, Nicola L., Tachezy, Jan, Betts, Emma L., Gentekaki, Eleni, van der Giezen, Mark, Clark, C. Graham, Jackson, Andrew P., Dacks, Joel B., Tsaousis, Anastasios D.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 19.06.2023
• Subjects: Animals; Blastocystis - genetics; comparative genomics; Eukaryota; flagella; Gastrointestinal Microbiome - genetics; Humans; microscopy; Mitochondria - genetics; Mitochondria - metabolism; mitochondrion-related organelle; Organelles - metabolism; parasite; peroxisome; protist; flagella; parasite; protist; peroxisome; microscopy; mitochondrion-related organelle; comparative genomics
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2023.05.025

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. [Display omitted] •A high-quality genome of Proteromonas was generated and compared with Blastocystis•The most highly reduced peroxisome to date is reported•The transition to specialized metabolism in Blastocystis is detailed•A co-evolutionary mechanism for mitochondrion and peroxisome dynamics is proposed The microscopic eukaryote Blastocystis is a frequent member of the animal gut microbiome, with altered biology adapted to this niche. Záhonová et al. characterize, at the genomic and cellular level, these adaptations by studying Proteromonas, the closest relative of Blastocystis. This yields insights about their metabolism and organellar evolution.