Genetic basis for the establishment of endosymbiosis in <i>Paramecium</i>

He, Ming; Wang, Jinfeng; Fan, Xinpeng; Liu, Xiaohui; Shi, Wenyu; Huang, Ning; Zhao, Fangqing; Miao, Miao

doi:10.1038/s41396-018-0341-4

Cited by 34 publications

(42 citation statements)

References 55 publications

(71 reference statements)

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“…So far, no homozygous P. bursaria diploid lines have been established since P. bursaria does not undergo autogamy (an autofertilization process) like other Paramecium species [87]. In a recent study reporting a draft of the P. bursaria genome [88], only about 7000 genes had orthologs in closely related P. caudatum, despite 17,226 genes being annotated. By combining population genomic data and gene expression profiles, we have established a functional genome of P. bursaria that contains 15,101 genes, 72% (10,841/15,101) of which share orthologs with P. caudatum (Fig.…”

Section: Discussionmentioning

confidence: 99%

Genome plasticity in Paramecium bursaria revealed by population genomics

Cheng

Liu

et al. 2020

BMC Biol

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Background Ciliates are an ancient and diverse eukaryotic group found in various environments. A unique feature of ciliates is their nuclear dimorphism, by which two types of nuclei, the diploid germline micronucleus (MIC) and polyploidy somatic macronucleus (MAC), are present in the same cytoplasm and serve different functions. During each sexual cycle, ciliates develop a new macronucleus in which newly fused genomes are extensively rearranged to generate functional minichromosomes. Interestingly, each ciliate species seems to have its way of processing genomes, providing a diversity of resources for studying genome plasticity and its regulation. Here, we sequenced and analyzed the macronuclear genome of different strains of Paramecium bursaria, a highly divergent species of the genus Paramecium which can stably establish endosymbioses with green algae. Results We assembled a high-quality macronuclear genome of P. bursaria and further refined genome annotation by comparing population genomic data. We identified several species-specific expansions in protein families and gene lineages that are potentially associated with endosymbiosis. Moreover, we observed an intensive chromosome breakage pattern that occurred during or shortly after sexual reproduction and contributed to highly variable gene dosage throughout the genome. However, patterns of copy number variation were highly correlated among genetically divergent strains, suggesting that copy number is adjusted by some regulatory mechanisms or natural selection. Further analysis showed that genes with low copy number variation among populations tended to function in basic cellular pathways, whereas highly variable genes were enriched in environmental response pathways. Conclusions We report programmed DNA rearrangements in the P. bursaria macronuclear genome that allow cells to adjust gene copy number globally according to individual gene functions. Our results suggest that large-scale gene copy number variation may represent an ancient mechanism for cells to adapt to different environments.

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Section: Discussionmentioning

confidence: 99%

Genome plasticity in Paramecium bursaria revealed by population genomics

Cheng

Liu

et al. 2020

BMC Biol

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“…Indeed, SMRT was employed in a hypotrich ciliate Oxytricha trifallax with highly fragmented genome, showing the ability to capture tiny nanochromosomes in single reads (Lindblad et al, 2019). It was also used for the high-quality and near-complete macronuclear genome assembly of another ciliate Paramecium bursaria (He et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses

Sheng

Duan

Cheng

et al. 2020

Sci. China Life Sci.

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The ciliate Tetrahymena thermophila has been a powerful model system for molecular and cellular biology. However, some investigations have been limited due to the incomplete closure and sequencing of the macronuclear genome assembly, which for many years has been stalled at 1,158 scaffolds, with large sections of unknown sequences (available in Tetrahymena Genome Database, TGD, http://ciliate.org/). Here we completed the first chromosome-level Tetrahymena macronuclear genome assembly, with approximately 300× long Single Molecule, Real-Time reads of the wild-type SB210 cells-the reference strain for the initial macronuclear genome sequencing project. All 181 chromosomes were capped with two telomeres and gaps were entirely closed. The completed genome shows significant improvements over the current assembly (TGD 2014) in both chromosome structure and sequence integrity. The majority of previously identified gene models shown in TGD were retained, with the addition of 36 new genes and 883 genes with modified gene models. The new genome and annotation were incorporated into TGD. This new genome allows for pursuit in some underexplored areas that were far more challenging previously; two of them, genome scrambling and chromosomal copy number, were investigated in this study. We expect that the completed macronuclear genome will facilitate many studies in Tetrahymena biology, as well as multiple lines of research in other eukaryotes.

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“…One of the most diverse and highly differentiated group among single‐celled microorganisms are ciliates, which emerged approximately one billion years ago (Parfrey, Lahr, Knoll, & Katz, ) and are abundant in diverse habitats across the globe, where they are among the most important components of food webs in aquatic ecosystems (Gao et al, ; Lynn, ). Ciliate diversity, physiology and abundance have been linked to studies of environmental change (Gong, Song, & Warren, ; Xu, Zhang, Jiang, & Yang, ), pollution monitoring (Gutiérrez, Martín‐González, Díaz, & Ortega, ; Jiang et al, ; Stoeck, Kochems, Forster, Lejzerowicz, & Pawlowski, ), biogeography (Foissner, Chao, & Katz, ; Liu et al, ; Petz, Valbonesi, Schiftner, Quesada, & Cynan Ellis‐Evans, ), adaptive evolution (Clark & Peck, ; He et al, ), cell biology (Jiang, Zhang, Vallesi, Yang, & Gao, ; Wang, Zhang, et al, ; Zheng et al, ) and epigenetics (Wang, Chen, Sheng, Liu, & Gao, ; Xiong et al, ; Zhao, Wang, Wang, Liu, & Gao, ).…”

Section: Introductionmentioning

confidence: 99%

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Chen

Jiang

Gao

et al. 2019

Molecular Ecology Resources

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As a model organism for studies of cell and environmental biology, the free‐living and cosmopolitan ciliate Euplotes vannus shows intriguing features like dual genome architecture (i.e., separate germline and somatic nuclei in each cell/organism), “gene‐sized” chromosomes, stop codon reassignment, programmed ribosomal frameshifting (PRF) and strong resistance to environmental stressors. However, the molecular mechanisms that account for these remarkable traits remain largely unknown. Here we report a combined analysis of de novo assembled high‐quality macronuclear (MAC; i.e., somatic) and partial micronuclear (MIC; i.e., germline) genome sequences for E. vannus, and transcriptome profiling data under varying conditions. The results demonstrate that: (a) the MAC genome contains more than 25,000 complete “gene‐sized” nanochromosomes (~85 Mb haploid genome size) with the N50 ~2.7 kb; (b) although there is a high frequency of frameshifting at stop codons UAA and UAG, we did not observe impaired transcript abundance as a result of PRF in this species as has been reported for other euplotids; (c) the sequence motif 5′‐TA‐3′ is conserved at nearly all internally‐eliminated sequence (IES) boundaries in the MIC genome, and chromosome breakage sites (CBSs) are duplicated and retained in the MAC genome; (d) by profiling the weighted correlation network of genes in the MAC under different environmental stressors, including nutrient scarcity, extreme temperature, salinity and the presence of ammonia, we identified gene clusters that respond to these external physical or chemical stimulations, and (e) we observed a dramatic increase in HSP70 gene transcription under salinity and chemical stresses but surprisingly, not under temperature changes; we link this temperature‐resistance to the evolved loss of temperature stress‐sensitive elements in regulatory regions. Together with the genome resources generated in this study, which are available online at Euplotes vannus Genome Database (http://evan.ciliate.org), these data provide molecular evidence for understanding the unique biology of highly adaptable microorganisms.

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Genetic basis for the establishment of endosymbiosis in Paramecium

Cited by 34 publications

References 55 publications

Genome plasticity in Paramecium bursaria revealed by population genomics

Genome plasticity in Paramecium bursaria revealed by population genomics

The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

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