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Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome

BACKGROUND: Each year, approximately 9.5 million metric tons of plastic waste enter the ocean with the potential to adversely impact all trophic levels. Until now, our understanding of the impact of plastic pollution on marine microorganisms has been largely restricted to the microbial assemblages t...

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Autores principales: Focardi, Amaranta, Moore, Lisa R., Raina, Jean-Baptiste, Seymour, Justin R., Paulsen, Ian T., Tetu, Sasha G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9590215/
https://www.ncbi.nlm.nih.gov/pubmed/36274162
http://dx.doi.org/10.1186/s40168-022-01369-x
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author Focardi, Amaranta
Moore, Lisa R.
Raina, Jean-Baptiste
Seymour, Justin R.
Paulsen, Ian T.
Tetu, Sasha G.
author_facet Focardi, Amaranta
Moore, Lisa R.
Raina, Jean-Baptiste
Seymour, Justin R.
Paulsen, Ian T.
Tetu, Sasha G.
author_sort Focardi, Amaranta
collection PubMed
description BACKGROUND: Each year, approximately 9.5 million metric tons of plastic waste enter the ocean with the potential to adversely impact all trophic levels. Until now, our understanding of the impact of plastic pollution on marine microorganisms has been largely restricted to the microbial assemblages that colonize plastic particles. However, plastic debris also leaches considerable amounts of chemical additives into the water, and this has the potential to impact key groups of planktonic marine microbes, not just those organisms attached to plastic surfaces. RESULTS: To investigate this, we explored the population and genetic level responses of a marine microbial community following exposure to leachate from a common plastic (polyvinyl chloride) or zinc, a specific plastic additive. Both the full mix of substances leached from polyvinyl chloride (PVC) and zinc alone had profound impacts on the taxonomic and functional diversity of our natural planktonic community. Microbial primary producers, both prokaryotic and eukaryotic, which comprise the base of the marine food web, were strongly impaired by exposure to plastic leachates, showing significant declines in photosynthetic efficiency, diversity, and abundance. Key heterotrophic taxa, such as SAR11, which are the most abundant planktonic organisms in the ocean, also exhibited significant declines in relative abundance when exposed to higher levels of PVC leachate. In contrast, many copiotrophic bacteria, including members of the Alteromonadales, dramatically increased in relative abundance under both exposure treatments. Moreover, functional gene and genome analyses, derived from metagenomes, revealed that PVC leachate exposure selects for fast-adapting, motile organisms, along with enrichment in genes usually associated with pathogenicity and an increased capacity to metabolize organic compounds leached from PVC. CONCLUSIONS: This study shows that substances leached from plastics can restructure marine microbial communities with the potential for significant impacts on trophodynamics and biogeochemical cycling. These findings substantially expand our understanding of the ways by which plastic pollution impact life in our oceans, knowledge which is particularly important given that the burden of plastic pollution in the marine environment is predicted to continue to rise. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01369-x.
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spelling pubmed-95902152022-10-25 Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome Focardi, Amaranta Moore, Lisa R. Raina, Jean-Baptiste Seymour, Justin R. Paulsen, Ian T. Tetu, Sasha G. Microbiome Research BACKGROUND: Each year, approximately 9.5 million metric tons of plastic waste enter the ocean with the potential to adversely impact all trophic levels. Until now, our understanding of the impact of plastic pollution on marine microorganisms has been largely restricted to the microbial assemblages that colonize plastic particles. However, plastic debris also leaches considerable amounts of chemical additives into the water, and this has the potential to impact key groups of planktonic marine microbes, not just those organisms attached to plastic surfaces. RESULTS: To investigate this, we explored the population and genetic level responses of a marine microbial community following exposure to leachate from a common plastic (polyvinyl chloride) or zinc, a specific plastic additive. Both the full mix of substances leached from polyvinyl chloride (PVC) and zinc alone had profound impacts on the taxonomic and functional diversity of our natural planktonic community. Microbial primary producers, both prokaryotic and eukaryotic, which comprise the base of the marine food web, were strongly impaired by exposure to plastic leachates, showing significant declines in photosynthetic efficiency, diversity, and abundance. Key heterotrophic taxa, such as SAR11, which are the most abundant planktonic organisms in the ocean, also exhibited significant declines in relative abundance when exposed to higher levels of PVC leachate. In contrast, many copiotrophic bacteria, including members of the Alteromonadales, dramatically increased in relative abundance under both exposure treatments. Moreover, functional gene and genome analyses, derived from metagenomes, revealed that PVC leachate exposure selects for fast-adapting, motile organisms, along with enrichment in genes usually associated with pathogenicity and an increased capacity to metabolize organic compounds leached from PVC. CONCLUSIONS: This study shows that substances leached from plastics can restructure marine microbial communities with the potential for significant impacts on trophodynamics and biogeochemical cycling. These findings substantially expand our understanding of the ways by which plastic pollution impact life in our oceans, knowledge which is particularly important given that the burden of plastic pollution in the marine environment is predicted to continue to rise. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01369-x. BioMed Central 2022-10-24 /pmc/articles/PMC9590215/ /pubmed/36274162 http://dx.doi.org/10.1186/s40168-022-01369-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Focardi, Amaranta
Moore, Lisa R.
Raina, Jean-Baptiste
Seymour, Justin R.
Paulsen, Ian T.
Tetu, Sasha G.
Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title_full Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title_fullStr Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title_full_unstemmed Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title_short Plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
title_sort plastic leachates impair picophytoplankton and dramatically reshape the marine microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9590215/
https://www.ncbi.nlm.nih.gov/pubmed/36274162
http://dx.doi.org/10.1186/s40168-022-01369-x
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