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).
-
Euplotes woodruffi genome sequencing and assemblyNCBI Bioproject, PRJNA781979.
-
etmemena sp. micronucleus genome sequencing and assemblyNCBI Bioproject, PRJNA694964.
-
Euplotes woodruffi RNA-seq for vegetative cellsNCBI Bioproject, PRJNA781602.
-
Tetmemena sp. RNA-seq for vegetative cellsNCBI Bioproject, PRJNA887426.
-
MDS-IES databasehttps://knot.math.usf.edu/mds_ies_db/2022/downloads.html.
-
MDS and IES annotations for Euplotes woodruff, Tetmemena sp. and Oxytricha trifallaxDryad Digital Repository, doi:10.5061/dryad.5dv41ns96.
-
Oxytricha trifallax micronucleus genomeGenbank GCA_000711775.1.
-
Oxytricha trifallax macronucleus genomeGenbank GCA_000295675.1.
-
Tetmemena sp. macronucleus genomeGenbank GCA_001273295.2.
-
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.
Metrics
-
- 2,844
- views
-
- 346
- downloads
-
- 10
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes
eLife 11:e82979.
https://doi.org/10.7554/eLife.82979
Further reading
-
- Evolutionary Biology
A major question in animal evolution is how genotypic and phenotypic changes are related, and another is when and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades, and an updated phylogeny for the phylum. We constructed 20 ancient molluscan linkage groups (MLGs) and show that these are relatively conserved in bivalve karyotypes, but in chitons they are subject to re-ordering, rearrangement, fusion, or partial duplication and vary even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.
-
- Evolutionary Biology
Mammalian gut microbiomes are highly dynamic communities that shape and are shaped by host aging, including age-related changes to host immunity, metabolism, and behavior. As such, gut microbial composition may provide valuable information on host biological age. Here, we test this idea by creating a microbiome-based age predictor using 13,563 gut microbial profiles from 479 wild baboons collected over 14 years. The resulting ‘microbiome clock’ predicts host chronological age. Deviations from the clock’s predictions are linked to some demographic and socio-environmental factors that predict baboon health and survival: animals who appear old-for-age tend to be male, sampled in the dry season (for females), and have high social status (both sexes). However, an individual’s ‘microbiome age’ does not predict the attainment of developmental milestones or lifespan. Hence, in our host population, gut microbiome age largely reflects current, as opposed to past, social and environmental conditions, and does not predict the pace of host development or host mortality risk. We add to a growing understanding of how age is reflected in different host phenotypes and what forces modify biological age in primates.
