Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

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...

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Published in:BMC Biology
Main Authors: Stephens, Timothy G., González-Pech, Raúl A., Cheng, Yuanyuan, Mohamed, Amin R., Burt, David W., Bhattacharya, Debashish, Ragan, Mark A., Chan, Cheong Xin
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central 2020
Subjects:
Online Access:https://espace.library.uq.edu.au/view/UQ:9dda3cb
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spelling ftunivqespace:oai:espace.library.uq.edu.au:UQ:9dda3cb 2023-05-15T13:42:01+02:00 Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions Stephens, Timothy G. González-Pech, Raúl A. Cheng, Yuanyuan Mohamed, Amin R. Burt, David W. Bhattacharya, Debashish Ragan, Mark A. Chan, Cheong Xin 2020-05-24 https://espace.library.uq.edu.au/view/UQ:9dda3cb eng eng BioMed Central doi:10.1186/s12915-020-00782-8 issn:1741-7007 orcid:0000-0001-9808-297X orcid:0000-0002-1747-9308 orcid:0000-0002-9991-1028 orcid:0000-0003-1672-7020 orcid:0000-0002-3729-8176 Not set RGP0030 DP150101875 DP190102474 NJ01170 Biotechnology Plant Science General Biochemistry Genetics and Molecular Biology Developmental Biology Cell Biology Physiology Ecology Evolution Behavior and Systematics Structural Biology General Agricultural and Biological Sciences 1100 Agricultural and Biological Sciences 1300 Biochemistry 1105 Ecology 1110 Plant Science 1305 Biotechnology 1307 Cell Biology 1309 Developmental Biology 1314 Physiology 1315 Structural Biology Journal Article 2020 ftunivqespace https://doi.org/10.1186/s12915-020-00782-8 2020-12-22T15:13:22Z 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.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.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. Article in Journal/Newspaper Antarc* Antarctica Arctic Phytoplankton The University of Queensland: UQ eSpace Arctic BMC Biology 18 1
institution Open Polar
collection The University of Queensland: UQ eSpace
op_collection_id ftunivqespace
language English
topic Biotechnology
Plant Science
General Biochemistry
Genetics and Molecular Biology
Developmental Biology
Cell Biology
Physiology
Ecology
Evolution
Behavior and Systematics
Structural Biology
General Agricultural and Biological Sciences
1100 Agricultural and Biological Sciences
1300 Biochemistry
1105 Ecology
1110 Plant Science
1305 Biotechnology
1307 Cell Biology
1309 Developmental Biology
1314 Physiology
1315 Structural Biology
spellingShingle Biotechnology
Plant Science
General Biochemistry
Genetics and Molecular Biology
Developmental Biology
Cell Biology
Physiology
Ecology
Evolution
Behavior and Systematics
Structural Biology
General Agricultural and Biological Sciences
1100 Agricultural and Biological Sciences
1300 Biochemistry
1105 Ecology
1110 Plant Science
1305 Biotechnology
1307 Cell Biology
1309 Developmental Biology
1314 Physiology
1315 Structural Biology
Stephens, Timothy G.
González-Pech, Raúl A.
Cheng, Yuanyuan
Mohamed, Amin R.
Burt, David W.
Bhattacharya, Debashish
Ragan, Mark A.
Chan, Cheong Xin
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions
topic_facet Biotechnology
Plant Science
General Biochemistry
Genetics and Molecular Biology
Developmental Biology
Cell Biology
Physiology
Ecology
Evolution
Behavior and Systematics
Structural Biology
General Agricultural and Biological Sciences
1100 Agricultural and Biological Sciences
1300 Biochemistry
1105 Ecology
1110 Plant Science
1305 Biotechnology
1307 Cell Biology
1309 Developmental Biology
1314 Physiology
1315 Structural Biology
description 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.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.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.
format Article in Journal/Newspaper
author Stephens, Timothy G.
González-Pech, Raúl A.
Cheng, Yuanyuan
Mohamed, Amin R.
Burt, David W.
Bhattacharya, Debashish
Ragan, Mark A.
Chan, Cheong Xin
author_facet Stephens, Timothy G.
González-Pech, Raúl A.
Cheng, Yuanyuan
Mohamed, Amin R.
Burt, David W.
Bhattacharya, Debashish
Ragan, Mark A.
Chan, Cheong Xin
author_sort Stephens, Timothy G.
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 BioMed Central
publishDate 2020
url https://espace.library.uq.edu.au/view/UQ:9dda3cb
geographic Arctic
geographic_facet Arctic
genre Antarc*
Antarctica
Arctic
Phytoplankton
genre_facet Antarc*
Antarctica
Arctic
Phytoplankton
op_relation doi:10.1186/s12915-020-00782-8
issn:1741-7007
orcid:0000-0001-9808-297X
orcid:0000-0002-1747-9308
orcid:0000-0002-9991-1028
orcid:0000-0003-1672-7020
orcid:0000-0002-3729-8176
Not set
RGP0030
DP150101875
DP190102474
NJ01170
op_doi https://doi.org/10.1186/s12915-020-00782-8
container_title BMC Biology
container_volume 18
container_issue 1
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