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

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, Natasha; Tachezy, Jan; Betts, Emma L.; Gentekaki, Eleni; Giezen, Mark van der; Clark, C. Graham; Jackson, Andrew P.; Dacks, Joel B.; Tsaousis, Anastasios D.

doi:10.1016/j.cub.2023.05.025

Cited by 6 publications

(8 citation statements)

References 90 publications

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“…Blastocystis has a unique morphology for a stramenopile, as it lacks stereotypical motile flagella and tubular hairs, and instead is spherical and non-motile. This morphology is reflected by massive gene loss in this organism; in our sequenced genomes, we find all Blastocystis isolates sequenced have experienced a dramatic loss of cilia and flagella related genes, as well as a substantial reduction of both dynein and kinesin microtubule motor proteins, in agreement with recent analyses 37 (Figure 6). These losses correlate with the morphological changes from stereotypical stramenopiles.…”

Section: Resultssupporting

confidence: 90%

“…The tortoise isolate was larger than any human-derived isolate at 32.2 Mb. BUSCO completeness estimates ranged from 43% to 61%, similar to previous analyses of Blastocystis and related species (Table 1) 31,37 . The BUSCO estimate for the larger-sized tortoise isolate, was comparable to the human isolates, indicating the difference in genome size is not due to increased genome completeness.…”

Section: Resultssupporting

confidence: 85%

“…To explore how the Blastocystis genus has emerged and diversified, we compared the Blastocystis genomes generated in this work to those of two other sequenced stramenopiles: Cafeteria burkhardae , a free-living heterotrophic marine flagellate 38 , and the recently sequenced Proteromonas lacertae , a reptile gut commensal closely related to Blastocystis 37 . These organisms are the closest relatives to Blastocystis that have sequenced genomes.…”

Section: Resultsmentioning

confidence: 99%

“…Proteins from Cafeteria burkhardae BVI (formerly Cafeteria roenbergensis BVI), and predicted proteins from Proteromonas lacertae were used for comparative genomics analyses 37,38 . The genome assembly, transcripts, and proteins for C. burkhardae was downloaded from GenBank under accession GCA_008330645.1.…”

Section: Methodsmentioning

confidence: 99%

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Hybrid assemblies of microbiomeBlastocystisprotists reveal evolutionary diversification reflecting host ecology

Lind,

McDonald,

Gerrick

et al. 2023

Preprint

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The most prevalent microbial eukaryote in the human gut isBlastocystis, an obligate commensal protist also common in many other vertebrates.Blastocystisis descended from free-living stramenopile ancestors; how it has adapted to thrive within humans and a wide range of hosts is unclear. Here, we cultivated sixBlastocystisstrains spanning the diversity of the genus and generated highly contiguous, annotated genomes with long-read DNA-seq, Hi-C, and RNA-seq. Comparative genomics between these strains and two closely related stramenopiles with different lifestyles, the lizard gut symbiontProteromonas lacertaeand the free-living marine flagellateCafeteria burkhardae, reveal the evolutionary history of theBlastocystisgenus. We find substantial gene content variability betweenBlastocystisstrains.Blastocystisisolated from an herbivorous tortoise has many plant carbohydrate metabolizing enzymes, some horizontally acquired from bacteria, likely reflecting fermentation within the host gut. In contrast, human- isolatedBlastocystishave gained many heat shock proteins, and we find numerous subtype- specific expansions of host-interfacing genes, including cell adhesion and cell surface glycan genes. In addition, we observe that human-isolatedBlastocystishave substantial changes in gene structure, including shortened introns and intergenic regions, as well as genes lacking canonical termination codons. Finally, our data indicate that the common ancestor ofBlastocystislost nearly all ancestral genes for heterokont flagella morphology, including cilia proteins, microtubule motor proteins, and ion channel proteins. Together, these findings underscore the huge functional variability within theBlastocystisgenus and provide candidate genes for the adaptations these lineages have undergone to thrive in the gut microbiomes of diverse vertebrates.

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Section: Resultssupporting

confidence: 90%

Section: Resultssupporting

confidence: 85%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Hybrid assemblies of microbiomeBlastocystisprotists reveal evolutionary diversification reflecting host ecology

Lind,

McDonald,

Gerrick

et al. 2023

Preprint

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“…Besides modifications or a complete loss of mitochondria, living in low-oxygen environments and/or living inside hosts typically impacts also peroxisomes. While in most anaerobic/microaerophilic species, including all previously investigated Metamonada, the peroxisomes are absent, both free-living and parasitic Archamoebae recently turned out to possess modified versions of this organelle [73–75], as does Proteromonas lacertae , a stramenopile that possesses the most reduced but seemingly functional peroxisomal organelle yet reported [76]. Specific genetic markers for the presence of peroxisomes are peroxins, a set of proteins involved in peroxisome biogenesis [77].…”

Section: Resultsmentioning

confidence: 99%

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Novák

Treitli

Pyrih

et al. 2022

Preprint

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Until recently, mitochondria were considered essential organelles impossible to truly lose in a lineage. This view changed in 2016, with the report that the oxymonadMonocercomonoides exilis, was the first known eukaryote without any mitochondrion. Questions remain, however, about whether this extends to the entire lineage and how this transition took place. Oxymonadida are a group of gut endobionts of insects, reptiles, and mammals. They are housed in the Preaxostyla (Metamonada), a protistan group that also contains free-living flagellates of generaTrimastixandParatrimastix. These latter two taxa harbor conspicuous mitochondrion-related organelles (MROs), while no mitochondria were reported for any oxymonad. Here we report genomic data sets of two Preaxostyla representatives, the free-livingParatrimastix pyriformisand the oxymonadBlattamonas nauphoetae. We note thatP. pyriformispossesses a set of unique or ancestral features among metamonads or eukaryotes, e.g.,p-cresol synthesis, UFMylation system, NAD+synthesis, selenium volatilization, or mercury methylation, demonstrating the biochemical versatility of this protist lineage. We performed thorough comparisons among all available genomic and transcriptomic data of Preaxostyla to corroborate both the absence of MRO in Oxymonadida and the nature of MROs present in other Preaxostyla and to decipher the evolutionary transition towards amitochondriality and endobiosis. Our results provide insights into the metabolic and endomembrane evolution, but most strikingly the data confirm the complete loss of mitochondria and every protein that has ever participated in the mitochondrion function for all three oxymonad species (M. exilis,B. nauphoetae, andStreblomastix strix) extending the amitochondriate status to the whole Oxymonadida.

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Characterization of the SUF FeS cluster synthesis machinery in the amitochondriate eukaryote Monocercomonoides exilis

Peña-Diaz,

Braymer,

Vacek

et al. 2024

Current Biology

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

Cited by 6 publications

References 90 publications

Hybrid assemblies of microbiomeBlastocystisprotists reveal evolutionary diversification reflecting host ecology

Hybrid assemblies of microbiomeBlastocystisprotists reveal evolutionary diversification reflecting host ecology

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Characterization of the SUF FeS cluster synthesis machinery in the amitochondriate eukaryote Monocercomonoides exilis

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