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Transposable element persistence via potential genome-level ecosystem engineering

BACKGROUND: The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). To date, the precise evolutionary and ecological conditions influencing TE accumulation remain poorly understood. Most previo...

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Autores principales: Kremer, Stefan C., Linquist, Stefan, Saylor, Brent, Elliott, Tyler A., Gregory, T. Ryan, Cottenie, Karl
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7236351/
https://www.ncbi.nlm.nih.gov/pubmed/32429843
http://dx.doi.org/10.1186/s12864-020-6763-1
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author Kremer, Stefan C.
Linquist, Stefan
Saylor, Brent
Elliott, Tyler A.
Gregory, T. Ryan
Cottenie, Karl
author_facet Kremer, Stefan C.
Linquist, Stefan
Saylor, Brent
Elliott, Tyler A.
Gregory, T. Ryan
Cottenie, Karl
author_sort Kremer, Stefan C.
collection PubMed
description BACKGROUND: The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). To date, the precise evolutionary and ecological conditions influencing TE accumulation remain poorly understood. Most previous attempts to identify these conditions have focused on evolutionary processes occurring at the host organism level, whereas we explore a TE ecology explanation. RESULTS: As an alternative (or additional) hypothesis, we propose that ecological mechanisms occurring within the host cell may contribute to patterns of TE accumulation. To test this idea, we conducted a series of experiments using a simulated asexual TE/host system. Each experiment tracked the accumulation rate for a given type of TE within a particular host genome. TEs in this system had a net deleterious effect on host fitness, which did not change over the course of experiments. As one might expect, in the majority of experiments TEs were either purged from the genome or drove the host population to extinction. However, in an intriguing handful of cases, TEs co-existed with hosts and accumulated to very large numbers. This tended to occur when TEs achieved a stable density relative to non-TE sequences in the genome (as opposed to reaching any particular absolute number). In our model, the only way to maintain a stable density was for TEs to generate new, inactive copies at a rate that balanced with the production of active (replicating) copies. CONCLUSIONS: From a TE ecology perspective, we suggest this could be interpreted as a case of ecosystem engineering within the genome, where TEs persist by creating their own “habitat”.
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spelling pubmed-72363512020-05-29 Transposable element persistence via potential genome-level ecosystem engineering Kremer, Stefan C. Linquist, Stefan Saylor, Brent Elliott, Tyler A. Gregory, T. Ryan Cottenie, Karl BMC Genomics Research Article BACKGROUND: The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). To date, the precise evolutionary and ecological conditions influencing TE accumulation remain poorly understood. Most previous attempts to identify these conditions have focused on evolutionary processes occurring at the host organism level, whereas we explore a TE ecology explanation. RESULTS: As an alternative (or additional) hypothesis, we propose that ecological mechanisms occurring within the host cell may contribute to patterns of TE accumulation. To test this idea, we conducted a series of experiments using a simulated asexual TE/host system. Each experiment tracked the accumulation rate for a given type of TE within a particular host genome. TEs in this system had a net deleterious effect on host fitness, which did not change over the course of experiments. As one might expect, in the majority of experiments TEs were either purged from the genome or drove the host population to extinction. However, in an intriguing handful of cases, TEs co-existed with hosts and accumulated to very large numbers. This tended to occur when TEs achieved a stable density relative to non-TE sequences in the genome (as opposed to reaching any particular absolute number). In our model, the only way to maintain a stable density was for TEs to generate new, inactive copies at a rate that balanced with the production of active (replicating) copies. CONCLUSIONS: From a TE ecology perspective, we suggest this could be interpreted as a case of ecosystem engineering within the genome, where TEs persist by creating their own “habitat”. BioMed Central 2020-05-19 /pmc/articles/PMC7236351/ /pubmed/32429843 http://dx.doi.org/10.1186/s12864-020-6763-1 Text en © The Author(s). 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Kremer, Stefan C.
Linquist, Stefan
Saylor, Brent
Elliott, Tyler A.
Gregory, T. Ryan
Cottenie, Karl
Transposable element persistence via potential genome-level ecosystem engineering
title Transposable element persistence via potential genome-level ecosystem engineering
title_full Transposable element persistence via potential genome-level ecosystem engineering
title_fullStr Transposable element persistence via potential genome-level ecosystem engineering
title_full_unstemmed Transposable element persistence via potential genome-level ecosystem engineering
title_short Transposable element persistence via potential genome-level ecosystem engineering
title_sort transposable element persistence via potential genome-level ecosystem engineering
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7236351/
https://www.ncbi.nlm.nih.gov/pubmed/32429843
http://dx.doi.org/10.1186/s12864-020-6763-1
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