The draft genome of Kipferlia bialata reveals reductive genome evolution in fornicate parasites

Tanifuji, Goro; Takabayashi, Shun; Kume, Keitaro; Takagi, Mizue; Nakayama, Takuro; Kamikawa, Ryoma; Inagaki, Yuji; Hashimoto, Takeji

doi:10.1371/journal.pone.0194487

Cited by 29 publications

(46 citation statements)

References 55 publications

(88 reference statements)

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“…Very few genes in G. intestinalis contain introns, with only eight known cis -spliced and four trans -spliced genes (five trans -introns) [44–46]. Similarly, only three cis - and no trans -introns were identified in the parasitic diplomonad S. salmonicida [35] , whereas the free-living fornicate K. bialata has on average seven cis -introns per protein encoding gene [31]. G. muris maintains homologues to the eight cis -spliced G. intestinalis genes, but has only three retained introns (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Here we describe the draft genome of G. muris , representing the first genome of any Giardia outside of the G. intestinalis species complex. We performed comparative genomics with free-living ( Kipferlia bialata [31]) and parasitic ( G. intestinalis [32–34] and S. salmonicida [35]) relatives to G. muris to determine how G. muris may have evolved into an intestinal pathogen of rodents.…”

Section: Introductionmentioning

confidence: 99%

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The compact genome of Giardia muris reveals important steps in the evolution of intestinal protozoan parasites

Jiménez-González

Einarsson

et al. 2020

Microbial Genomics

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Diplomonad parasites of the genus Giardia have adapted to colonizing different hosts, most notably the intestinal tract of mammals. The human-pathogenic Giardia species, Giardia intestinalis, has been extensively studied at the genome and gene expression level, but no such information is available for other Giardia species. Comparative data would be particularly valuable for Giardia muris, which colonizes mice and is commonly used as a prototypic in vivo model for investigating host responses to intestinal parasitic infection. Here we report the draft-genome of G. muris. We discovered a highly streamlined genome, amongst the most densely encoded ever described for a nuclear eukaryotic genome. G. muris and G. intestinalis share many known or predicted virulence factors, including cysteine proteases and a large repertoire of cysteine-rich surface proteins involved in antigenic variation. Different to G. intestinalis, G. muris maintains tandem arrays of pseudogenized surface antigens at the telomeres, whereas intact surface antigens are present centrally in the chromosomes. The two classes of surface antigens engage in genetic exchange. Reconstruction of metabolic pathways from the G. muris genome suggest significant metabolic differences to G. intestinalis. Additionally, G. muris encodes proteins that might be used to modulate the prokaryotic microbiota. The responsible genes have been introduced in the Giardia genus via lateral gene transfer from prokaryotic sources. Our findings point to important evolutionary steps in the Giardia genus as it adapted to different hosts and it provides a powerful foundation for mechanistic exploration of host–pathogen interaction in the G. muris–mouse pathosystem.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The compact genome of Giardia muris reveals important steps in the evolution of intestinal protozoan parasites

Jiménez-González

Einarsson

et al. 2020

Microbial Genomics

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“…For the second RNA-seq run, we separated PAP020 cells from the bacterial cells in the culture medium by a gradient centrifugation using Optiprep (Axis Shield), as reported previously (Tanifuji et al 2018), with slight modifications (the Optiprep solution containing the eukaryotic cells and bacteria was centrifuged at 2,000 g for 20 min, instead of 800 g for 20 min). Total RNA was extracted from the harvested eukaryote-enriched fraction, using TRIzol by following the manufacturer’s protocol.…”

Section: Methodsmentioning

confidence: 99%

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Yazaki

Kume

Shiratori

et al. 2019

Preprint

Self Cite

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23Running head: Phylogeny and putative MRO functions in a new metamonad clade. 25Abstract 28 We here report the phylogenetic position of barthelonids, small anaerobic flagellates 29 previously examined using light microscopy alone. Barthelona spp. were isolated from 30 geographically distinct regions and we established five laboratory strains. Transcriptomic data 31 generated from one Barthelona strain (PAP020) was used for large-scale, multi-gene 32 phylogenetic (phylogenomic) analyses. Our analyses robustly placed strain PAP020 at the 33 base of the Fornicata clade, indicating that barthelonids represent a deep-branching 34 Metamonad clade. Considering the anaerobic/microaerophilic nature of barthelonids and 35 preliminary electron microscopy observations on strain PAP020, we suspected that 36 barthelonids possess functionally and structurally reduced mitochondria (i.e. mitochondrion-37 related organelles or MROs). The metabolic pathways localized in the MRO of strain PAP020 38 were predicted based on its transcriptomic data and compared with those in the MROs of 39 fornicates. Strain PAP020 is most likely incapable of generating ATP in the MRO, as no 40 mitochondrial/MRO enzymes involved in substrate-level phosphorylation were detected. 41 Instead, we detected the putative cytosolic ATP-generating enzyme (acetyl-CoA synthetase), 42 suggesting that strain PAP020 depends on ATP generated in the cytosol. We propose two 43 separate losses of substrate-level phosphorylation from the MRO in the clade containing 44 barthelonids and (other) fornicates.45 46

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“…Within Excavata, mitogenomes are extremely diverse (Figure 2). The mitogenomes of Jakobida are the richest in gene content 114,137 and the most similar to the transcriptional and translational machinery operons in bacterial genomes 138 ; those of Heterolobosea are compact and gene-rich 139 ; those of some Euglenozoa are arranged in specialized structures called kinetoplasts 140 and in Metamonada are simply absent as species either have highly reduced versions of mitochondria called mitochondrion-related organelles 141,142 or completely lack them 143 because of their adaptation to anaerobic environments. Jakobid mitogenomes are mostly circular, of 67 to 100 Kb, and share a large core set of genes 137,144,145 , which include the OXPHOS system protein-coding genes reported for Marophrys sp.…”

Section: Other Eukaryote Mitogenome Structuresmentioning

confidence: 99%

Recent advances in understanding mitochondrial genome diversity

Zardoya

2020

F1000Res

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Ever since its discovery, the double-stranded DNA contained in the mitochondria of eukaryotes has fascinated researchers because of its bacterial endosymbiotic origin, crucial role in encoding subunits of the respiratory complexes, compact nature, and specific inheritance mechanisms. In the last few years, high-throughput sequencing techniques have accelerated the sequencing of mitochondrial genomes (mitogenomes) and uncovered the great diversity of organizations, gene contents, and modes of replication and transcription found in living eukaryotes. Some early divergent lineages of unicellular eukaryotes retain certain synteny and gene content resembling those observed in the genomes of alphaproteobacteria (the inferred closest living group of mitochondria), whereas others adapted to anaerobic environments have drastically reduced or even lost the mitogenome. In the three main multicellular lineages of eukaryotes, mitogenomes have pursued diverse evolutionary trajectories in which different types of molecules (circular versus linear and single versus multipartite), gene structures (with or without self-splicing introns), gene contents, gene orders, genetic codes, and transfer RNA editing mechanisms have been selected. Whereas animals have evolved a rather compact mitochondrial genome between 11 and 50 Kb in length with a highly conserved gene content in bilaterians, plants exhibit large mitochondrial genomes of 66 Kb to 11.3 Mb with large intergenic repetitions prone to recombination, and fungal mitogenomes have intermediate sizes of 12 to 236 Kb.

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The draft genome of Kipferlia bialata reveals reductive genome evolution in fornicate parasites

Cited by 29 publications

References 55 publications

The compact genome of Giardia muris reveals important steps in the evolution of intestinal protozoan parasites

The compact genome of Giardia muris reveals important steps in the evolution of intestinal protozoan parasites

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Recent advances in understanding mitochondrial genome diversity

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