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Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors

The formation, propagation, and maintenance of harmful algal blooms are of interest due to their negative effects on marine life and human health. Some bloom-forming algae utilize allelopathy, the release of compounds that inhibit competitors, to exclude other species dependent on a common pool of l...

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Autores principales: Poulin, Remington X., Hogan, Scott, Poulson-Ellestad, Kelsey L., Brown, Emily, Fernández, Facundo M., Kubanek, Julia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6015087/
https://www.ncbi.nlm.nih.gov/pubmed/29934632
http://dx.doi.org/10.1038/s41598-018-27845-9
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author Poulin, Remington X.
Hogan, Scott
Poulson-Ellestad, Kelsey L.
Brown, Emily
Fernández, Facundo M.
Kubanek, Julia
author_facet Poulin, Remington X.
Hogan, Scott
Poulson-Ellestad, Kelsey L.
Brown, Emily
Fernández, Facundo M.
Kubanek, Julia
author_sort Poulin, Remington X.
collection PubMed
description The formation, propagation, and maintenance of harmful algal blooms are of interest due to their negative effects on marine life and human health. Some bloom-forming algae utilize allelopathy, the release of compounds that inhibit competitors, to exclude other species dependent on a common pool of limiting resources. Allelopathy is hypothesized to affect bloom dynamics and is well established in the red tide dinoflagellate Karenia brevis. K. brevis typically suppresses competitor growth rather than being acutely toxic to other algae. When we investigated the effects of allelopathy on two competitors, Asterionellopsis glacialis and Thalassiosira pseudonana, using nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry (MS)-based metabolomics, we found that the lipidomes of both species were significantly altered. However, A. glacialis maintained a more robust metabolism in response to K. brevis allelopathy whereas T. pseudonana exhibited significant alterations in lipid synthesis, cell membrane integrity, and photosynthesis. Membrane-associated lipids were significantly suppressed for T. pseudonana exposed to allelopathy such that membranes of living cells became permeable. K. brevis allelopathy appears to target lipid biosynthesis affecting multiple physiological pathways suggesting that exuded compounds have the ability to significantly alter competitor physiology, giving K. brevis an edge over sensitive species.
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spelling pubmed-60150872018-07-06 Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors Poulin, Remington X. Hogan, Scott Poulson-Ellestad, Kelsey L. Brown, Emily Fernández, Facundo M. Kubanek, Julia Sci Rep Article The formation, propagation, and maintenance of harmful algal blooms are of interest due to their negative effects on marine life and human health. Some bloom-forming algae utilize allelopathy, the release of compounds that inhibit competitors, to exclude other species dependent on a common pool of limiting resources. Allelopathy is hypothesized to affect bloom dynamics and is well established in the red tide dinoflagellate Karenia brevis. K. brevis typically suppresses competitor growth rather than being acutely toxic to other algae. When we investigated the effects of allelopathy on two competitors, Asterionellopsis glacialis and Thalassiosira pseudonana, using nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry (MS)-based metabolomics, we found that the lipidomes of both species were significantly altered. However, A. glacialis maintained a more robust metabolism in response to K. brevis allelopathy whereas T. pseudonana exhibited significant alterations in lipid synthesis, cell membrane integrity, and photosynthesis. Membrane-associated lipids were significantly suppressed for T. pseudonana exposed to allelopathy such that membranes of living cells became permeable. K. brevis allelopathy appears to target lipid biosynthesis affecting multiple physiological pathways suggesting that exuded compounds have the ability to significantly alter competitor physiology, giving K. brevis an edge over sensitive species. Nature Publishing Group UK 2018-06-22 /pmc/articles/PMC6015087/ /pubmed/29934632 http://dx.doi.org/10.1038/s41598-018-27845-9 Text en © The Author(s) 2018 Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Poulin, Remington X.
Hogan, Scott
Poulson-Ellestad, Kelsey L.
Brown, Emily
Fernández, Facundo M.
Kubanek, Julia
Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title_full Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title_fullStr Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title_full_unstemmed Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title_short Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
title_sort karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6015087/
https://www.ncbi.nlm.nih.gov/pubmed/29934632
http://dx.doi.org/10.1038/s41598-018-27845-9
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