Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions
Abstract Background Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some ca...
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doaj-7b3cf18ce2bc405e9d83b29a04a48e782020-11-25T03:09:20ZengBMCBMC Biology1741-70072020-05-0118112110.1186/s12915-020-00782-8Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functionsTimothy G. Stephens0Raúl A. González-Pech1Yuanyuan Cheng2Amin R. Mohamed3David W. Burt4Debashish Bhattacharya5Mark A. Ragan6Cheong Xin Chan7Institute for Molecular Bioscience, The University of QueenslandInstitute for Molecular Bioscience, The University of QueenslandUQ Genomics Initiative, The University of QueenslandCommonwealth Scientific and Industrial Research Organisation (CSIRO) Agriculture and Food, Queensland Bioscience PrecinctUQ Genomics, The University of QueenslandDepartment of Biochemistry and Microbiology, Rutgers UniversityInstitute for Molecular Bioscience, The University of QueenslandInstitute for Molecular Bioscience, The University of QueenslandAbstract Background Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxa that have smaller genome size ranges, while genomic information from more diverse free-living species is still lacking. Results Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which ~40% are in unidirectional gene clusters and ~25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates. Conclusions Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution.http://link.springer.com/article/10.1186/s12915-020-00782-8DinoflagellatesGenomicsGenome evolutionPolarella glacialisCold adaptation |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Timothy G. Stephens Raúl A. González-Pech Yuanyuan Cheng Amin R. Mohamed David W. Burt Debashish Bhattacharya Mark A. Ragan Cheong Xin Chan |
spellingShingle |
Timothy G. Stephens Raúl A. González-Pech Yuanyuan Cheng Amin R. Mohamed David W. Burt Debashish Bhattacharya Mark A. Ragan Cheong Xin Chan Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions BMC Biology Dinoflagellates Genomics Genome evolution Polarella glacialis Cold adaptation |
author_facet |
Timothy G. Stephens Raúl A. González-Pech Yuanyuan Cheng Amin R. Mohamed David W. Burt Debashish Bhattacharya Mark A. Ragan Cheong Xin Chan |
author_sort |
Timothy G. Stephens |
title |
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
title_short |
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
title_full |
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
title_fullStr |
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
title_full_unstemmed |
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
title_sort |
genomes of the dinoflagellate polarella glacialis encode tandemly repeated single-exon genes with adaptive functions |
publisher |
BMC |
series |
BMC Biology |
issn |
1741-7007 |
publishDate |
2020-05-01 |
description |
Abstract Background Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxa that have smaller genome size ranges, while genomic information from more diverse free-living species is still lacking. Results Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which ~40% are in unidirectional gene clusters and ~25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates. Conclusions Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution. |
topic |
Dinoflagellates Genomics Genome evolution Polarella glacialis Cold adaptation |
url |
http://link.springer.com/article/10.1186/s12915-020-00782-8 |
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