Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations

Spliceosomal introns are a hallmark of eukaryotic genes that are hypothesized to play important roles in genome evolution but have poorly understood origins. Although most introns lack sequence homology to each other, new families of spliceosomal introns that are repeated hundreds of times in indivi...

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Published in:Molecular Biology and Evolution
Main Authors: Simmons, Melinda P., Bachy, Charles, Sudek, Sebastian, van Baren, Marijke J., Sudek, Lisa, Ares, Manuel, Worden, Alexandra Z.
Format: Text
Language:English
Published: Oxford University Press 2015
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4540971/
http://www.ncbi.nlm.nih.gov/pubmed/25998521
https://doi.org/10.1093/molbev/msv122
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spelling ftpubmed:oai:pubmedcentral.nih.gov:4540971 2023-05-15T14:01:26+02:00 Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations Simmons, Melinda P. Bachy, Charles Sudek, Sebastian van Baren, Marijke J. Sudek, Lisa Ares, Manuel Worden, Alexandra Z. 2015-09 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4540971/ http://www.ncbi.nlm.nih.gov/pubmed/25998521 https://doi.org/10.1093/molbev/msv122 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4540971/ http://www.ncbi.nlm.nih.gov/pubmed/25998521 http://dx.doi.org/10.1093/molbev/msv122 © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com CC-BY-NC Fast Track Text 2015 ftpubmed https://doi.org/10.1093/molbev/msv122 2015-08-23T00:11:18Z Spliceosomal introns are a hallmark of eukaryotic genes that are hypothesized to play important roles in genome evolution but have poorly understood origins. Although most introns lack sequence homology to each other, new families of spliceosomal introns that are repeated hundreds of times in individual genomes have recently been discovered in a few organisms. The prevalence and conservation of these introner elements (IEs) or introner-like elements in other taxa, as well as their evolutionary relationships to regular spliceosomal introns, are still unknown. Here, we systematically investigate introns in the widespread marine green alga Micromonas and report new families of IEs, numerous intron presence–absence polymorphisms, and potential intron insertion hot-spots. The new families enabled identification of conserved IE secondary structure features and establishment of a novel general model for repetitive intron proliferation across genomes. Despite shared secondary structure, the IE families from each Micromonas lineage bear no obvious sequence similarity to those in the other lineages, suggesting that their appearance is intimately linked with the process of speciation. Two of the new IE families come from an Arctic culture (Micromonas Clade E2) isolated from a polar region where abundance of this alga is increasing due to climate induced changes. The same two families were detected in metagenomic data from Antarctica—a system where Micromonas has never before been reported. Strikingly high identity between the Arctic isolate and Antarctic coding sequences that flank the IEs suggests connectivity between populations in the two polar systems that we postulate occurs through deep-sea currents. Recovery of Clade E2 sequences in North Atlantic Deep Waters beneath the Gulf Stream supports this hypothesis. Our research illuminates the dynamic relationships between an unusual class of repetitive introns, genome evolution, speciation, and global distribution of this sentinel marine alga. Text Antarc* Antarctic Antarctica Arctic North Atlantic PubMed Central (PMC) Antarctic Arctic Molecular Biology and Evolution 32 9 2219 2235
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Fast Track
spellingShingle Fast Track
Simmons, Melinda P.
Bachy, Charles
Sudek, Sebastian
van Baren, Marijke J.
Sudek, Lisa
Ares, Manuel
Worden, Alexandra Z.
Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
topic_facet Fast Track
description Spliceosomal introns are a hallmark of eukaryotic genes that are hypothesized to play important roles in genome evolution but have poorly understood origins. Although most introns lack sequence homology to each other, new families of spliceosomal introns that are repeated hundreds of times in individual genomes have recently been discovered in a few organisms. The prevalence and conservation of these introner elements (IEs) or introner-like elements in other taxa, as well as their evolutionary relationships to regular spliceosomal introns, are still unknown. Here, we systematically investigate introns in the widespread marine green alga Micromonas and report new families of IEs, numerous intron presence–absence polymorphisms, and potential intron insertion hot-spots. The new families enabled identification of conserved IE secondary structure features and establishment of a novel general model for repetitive intron proliferation across genomes. Despite shared secondary structure, the IE families from each Micromonas lineage bear no obvious sequence similarity to those in the other lineages, suggesting that their appearance is intimately linked with the process of speciation. Two of the new IE families come from an Arctic culture (Micromonas Clade E2) isolated from a polar region where abundance of this alga is increasing due to climate induced changes. The same two families were detected in metagenomic data from Antarctica—a system where Micromonas has never before been reported. Strikingly high identity between the Arctic isolate and Antarctic coding sequences that flank the IEs suggests connectivity between populations in the two polar systems that we postulate occurs through deep-sea currents. Recovery of Clade E2 sequences in North Atlantic Deep Waters beneath the Gulf Stream supports this hypothesis. Our research illuminates the dynamic relationships between an unusual class of repetitive introns, genome evolution, speciation, and global distribution of this sentinel marine alga.
format Text
author Simmons, Melinda P.
Bachy, Charles
Sudek, Sebastian
van Baren, Marijke J.
Sudek, Lisa
Ares, Manuel
Worden, Alexandra Z.
author_facet Simmons, Melinda P.
Bachy, Charles
Sudek, Sebastian
van Baren, Marijke J.
Sudek, Lisa
Ares, Manuel
Worden, Alexandra Z.
author_sort Simmons, Melinda P.
title Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
title_short Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
title_full Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
title_fullStr Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
title_full_unstemmed Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations
title_sort intron invasions trace algal speciation and reveal nearly identical arctic and antarctic micromonas populations
publisher Oxford University Press
publishDate 2015
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4540971/
http://www.ncbi.nlm.nih.gov/pubmed/25998521
https://doi.org/10.1093/molbev/msv122
geographic Antarctic
Arctic
geographic_facet Antarctic
Arctic
genre Antarc*
Antarctic
Antarctica
Arctic
North Atlantic
genre_facet Antarc*
Antarctic
Antarctica
Arctic
North Atlantic
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4540971/
http://www.ncbi.nlm.nih.gov/pubmed/25998521
http://dx.doi.org/10.1093/molbev/msv122
op_rights © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
http://creativecommons.org/licenses/by-nc/4.0/
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
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op_doi https://doi.org/10.1093/molbev/msv122
container_title Molecular Biology and Evolution
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