Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes
- Columbia University, United States
- Universidad del Norte, Colombia
- Pacific Biosciences, United States
- University of South Florida, United States
Abstract
Ciliates are microbial eukaryotes that undergo extensive programmed genome rearrangement, a natural genome editing process that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome, whose assembly during development requires hundreds of thousands of precise programmed DNA joining events, representing the most complex genome dynamics of any known organism. Here we study the emergence of such complex genomes by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage. This study compares six genomes from three species, the germline and somatic genomes for Euplotes woodruffi, Tetmemena sp., and the model ciliate Oxytricha trifallax. To complement existing data, we sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi, which provides an outgroup, and the germline genome of Tetmemena sp.. We find that the germline genome of Tetmemena is as massively scrambled and interrupted as Oxytricha's : 13.6% of its gene loci require programmed translocations and/or inversions, with some genes requiring hundreds of precise gene editing events during development. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but only roughly half as many loci (7.3%) are scrambled. Furthermore, its scrambled genes are less complex, together supporting the position of Euplotes as a possible evolutionary intermediate in this lineage, in the process of accumulating complex evolutionary genome rearrangements, all of which require extensive repair to assemble functional coding regions. Comparative analysis also reveals that scrambled loci are often associated with local duplications, supporting a gradual model for the origin of complex, scrambled genomes via many small events of DNA duplication and decay.
Data availability
Custom scripts are public on https://github.com/yifeng-evo/Oxytricha_Tetmemena_Euplotes. DNA-seq reads and genome assemblies are available at GenBank under Bioprojects PRJNA694964 (Tetmemena sp.) and PRJNA781979 (Euplotes woodruffi). Genbank accession numbers for genomes are JAJKFJ000000000 (Tetmemena sp. Micronucleus genome), JAJLLS000000000 (Euplotes woodruffi Micronucleus genome), and JAJLLT000000000 (Euplotes woodruffi Macronucleus genome).Three replicates of RNA-seq reads for vegetative cells are available at GenBank under accession numbers of SRR21815378, SRR21815379, SRR21815380 for E. woodruffi and SRR21817702, SRR21817703 and SRR21817704 for Tetmemena sp..MDSs annotations for three species are available at https://doi.org/10.5061/dryad.5dv41ns96 and https://knot.math.usf.edu/mds_ies_db/2022/downloads.html (please select species from the drop-down menu).
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Euplotes woodruffi genome sequencing and assemblyNCBI Bioproject, PRJNA781979.
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etmemena sp. micronucleus genome sequencing and assemblyNCBI Bioproject, PRJNA694964.
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Euplotes woodruffi RNA-seq for vegetative cellsNCBI Bioproject, PRJNA781602.
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Tetmemena sp. RNA-seq for vegetative cellsNCBI Bioproject, PRJNA887426.
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MDS-IES databasehttps://knot.math.usf.edu/mds_ies_db/2022/downloads.html.
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MDS and IES annotations for Euplotes woodruff, Tetmemena sp. and Oxytricha trifallaxDryad Digital Repository, doi:10.5061/dryad.5dv41ns96.
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Oxytricha trifallax micronucleus genomeGenbank GCA_000711775.1.
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Oxytricha trifallax macronucleus genomeGenbank GCA_000295675.1.
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Tetmemena sp. macronucleus genomeGenbank GCA_001273295.2.
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Oxytricha trifallax RNA-seq for vegetative cellsNCBI SRA SRX5944382, SRX5944383 and SRX5944384.
Article and author information
Author details
Funding
National Institutes of Health (R35GM122555)
- Yi Feng
National Science Foundation (DMS1764366)
- Yi Feng
Pew Latin American Fellows Program (no)
- Rafik Neme
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Feng et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes
eLife 11:e82979.
https://doi.org/10.7554/eLife.82979
Further reading
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- Evolutionary Biology
Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation by distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60km2 per generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.
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- Evolutionary Biology
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than ten alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognized.
