Exposure to the Florida red tide dinoflagellate, Karenia brevis, and its associated brevetoxins induces ecophysiological and proteomic alterations in Porites astreoides

As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to better understand the complex processes that diminish coral populations. This study investigated the impacts of the Florida red tide dinoflagellat...

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Published inPloS one Vol. 15; no. 2; p. e0228414
Main Authors Reynolds, David A, Yoo, Mi-Jeong, Dixson, Danielle L, Ross, Cliff
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.02.2020
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Abstract As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to better understand the complex processes that diminish coral populations. This study investigated the impacts of the Florida red tide dinoflagellate Karenia brevis and associated brevetoxins on selected facets of coral biology using Porites astreoides as a model system. When provided with choice assays, P. astreoides larvae were shown to actively avoid seawater containing red tide (5×105 cells L-1-7.6×106 cells L-1) or purified brevetoxins (0.018 μg mL-1 brevetoxin-2 and 0.0018 μg mL-1 brevetoxin-3). However, forced exposure to similar treatments induced time-dependent physiological and behavioral changes that were captured by PAM fluorometry and settlement and survival assays, respectively. Adult fragments of P. astreoides exposed to red tide or associated brevetoxins displayed signs of proteomic alterations that were characterized by the use of an iTRAQ-based quantitative proteomic analysis. The novel use of this technique with P. astreoides demonstrated that protein regulation was highly contingent upon biological versus chemical treatment (i.e. live K. brevis vs. solely brevetoxin exposure) and that several broad pathways associated with cell stress were affected including redox homeostasis, protein folding, energy metabolism and reactive oxygen species production. The results herein provide new insight into the ecology, behavior and sublethal stress of reef-building corals in response to K. brevis exposure and underscore the importance of recognizing the potential of red tide to act as a regional stressor to these important foundation species.
AbstractList As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to better understand the complex processes that diminish coral populations. This study investigated the impacts of the Florida red tide dinoflagellate Karenia brevis and associated brevetoxins on selected facets of coral biology using Porites astreoides as a model system. When provided with choice assays, P. astreoides larvae were shown to actively avoid seawater containing red tide (5×105 cells L-1-7.6×106 cells L-1) or purified brevetoxins (0.018 μg mL-1 brevetoxin-2 and 0.0018 μg mL-1 brevetoxin-3). However, forced exposure to similar treatments induced time-dependent physiological and behavioral changes that were captured by PAM fluorometry and settlement and survival assays, respectively. Adult fragments of P. astreoides exposed to red tide or associated brevetoxins displayed signs of proteomic alterations that were characterized by the use of an iTRAQ-based quantitative proteomic analysis. The novel use of this technique with P. astreoides demonstrated that protein regulation was highly contingent upon biological versus chemical treatment (i.e. live K. brevis vs. solely brevetoxin exposure) and that several broad pathways associated with cell stress were affected including redox homeostasis, protein folding, energy metabolism and reactive oxygen species production. The results herein provide new insight into the ecology, behavior and sublethal stress of reef-building corals in response to K. brevis exposure and underscore the importance of recognizing the potential of red tide to act as a regional stressor to these important foundation species.
As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to better understand the complex processes that diminish coral populations. This study investigated the impacts of the Florida red tide dinoflagellate Karenia brevis and associated brevetoxins on selected facets of coral biology using Porites astreoides as a model system. When provided with choice assays, P. astreoides larvae were shown to actively avoid seawater containing red tide (5x10.sup.5 cells L.sup.-1 -7.6x10.sup.6 cells L.sup.-1) or purified brevetoxins (0.018 [mu]g mL.sup.-1 brevetoxin-2 and 0.0018 [mu]g mL.sup.-1 brevetoxin-3). However, forced exposure to similar treatments induced time-dependent physiological and behavioral changes that were captured by PAM fluorometry and settlement and survival assays, respectively. Adult fragments of P. astreoides exposed to red tide or associated brevetoxins displayed signs of proteomic alterations that were characterized by the use of an iTRAQ-based quantitative proteomic analysis. The novel use of this technique with P. astreoides demonstrated that protein regulation was highly contingent upon biological versus chemical treatment (i.e. live K. brevis vs. solely brevetoxin exposure) and that several broad pathways associated with cell stress were affected including redox homeostasis, protein folding, energy metabolism and reactive oxygen species production. The results herein provide new insight into the ecology, behavior and sublethal stress of reef-building corals in response to K. brevis exposure and underscore the importance of recognizing the potential of red tide to act as a regional stressor to these important foundation species.
As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to better understand the complex processes that diminish coral populations. This study investigated the impacts of the Florida red tide dinoflagellate Karenia brevis and associated brevetoxins on selected facets of coral biology using Porites astreoides as a model system. When provided with choice assays, P . astreoides larvae were shown to actively avoid seawater containing red tide (5×10 5 cells L -1 –7.6×10 6 cells L -1 ) or purified brevetoxins (0.018 μg mL -1 brevetoxin-2 and 0.0018 μg mL -1 brevetoxin-3). However, forced exposure to similar treatments induced time-dependent physiological and behavioral changes that were captured by PAM fluorometry and settlement and survival assays, respectively. Adult fragments of P . astreoides exposed to red tide or associated brevetoxins displayed signs of proteomic alterations that were characterized by the use of an iTRAQ-based quantitative proteomic analysis. The novel use of this technique with P . astreoides demonstrated that protein regulation was highly contingent upon biological versus chemical treatment ( i . e . live K . brevis vs. solely brevetoxin exposure) and that several broad pathways associated with cell stress were affected including redox homeostasis, protein folding, energy metabolism and reactive oxygen species production. The results herein provide new insight into the ecology, behavior and sublethal stress of reef-building corals in response to K . brevis exposure and underscore the importance of recognizing the potential of red tide to act as a regional stressor to these important foundation species.
Audience Academic
Author Ross, Cliff
Yoo, Mi-Jeong
Reynolds, David A
Dixson, Danielle L
AuthorAffiliation 1 Department of Biology, University of North Florida, Jacksonville, Florida, United States of America
2 Department of Biology, Clarkson University, Potsdam, New York, United States of America
Living Oceans Foundation, TAIWAN
3 School of Marine Science and Policy, University of Delaware, Lewes, Delaware, United States of America
AuthorAffiliation_xml – name: Living Oceans Foundation, TAIWAN
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  surname: Reynolds
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  organization: Department of Biology, University of North Florida, Jacksonville, Florida, United States of America
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32032360$$D View this record in MEDLINE/PubMed
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Copyright COPYRIGHT 2020 Public Library of Science
2020 Reynolds et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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PublicationDate 2020-02-07
PublicationDateYYYYMMDD 2020-02-07
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Snippet As reef-building corals are increasingly being exposed to persistent threats that operate on both regional and global scales, there is a pressing need to...
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SubjectTerms Animal behavior
Animals
Biology
Biology and Life Sciences
Brevetoxins
Cellular stress response
Chemical analysis
Chemical treatment
Coral reefs
Corals
Dinoflagellates
Dinoflagellida - pathogenicity
Earth Sciences
Ecological effects
Ecology
Ecology and Environmental Sciences
Ecosystem
Energy metabolism
Environmental Exposure - adverse effects
Exposure
Fluorimetry
Fluorometry
Gene expression
Genomes
Harmful Algal Bloom - drug effects
Harmful Algal Bloom - physiology
Homeostasis
Karenia brevis
Larva - drug effects
Larva - growth & development
Larva - metabolism
Larvae
Marine toxins
Marine Toxins - toxicity
Metabolism
Microorganisms
Novels
Organic chemistry
Oxocins - toxicity
Oxygen
Peptides
Population studies
Porites astreoides
Protein folding
Protein turnover
Proteins
Proteome - analysis
Proteomics
Reactive oxygen species
Red tides
Research and Analysis Methods
Seawater
Tides
Time
Time dependence
Water analysis
Water pollution effects
Water quality
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Title Exposure to the Florida red tide dinoflagellate, Karenia brevis, and its associated brevetoxins induces ecophysiological and proteomic alterations in Porites astreoides
URI https://www.ncbi.nlm.nih.gov/pubmed/32032360
https://www.proquest.com/docview/2352320932
https://search.proquest.com/docview/2352637731
https://pubmed.ncbi.nlm.nih.gov/PMC7006924
https://doaj.org/article/d5ad98f878b84164a6562e7d20e18aeb
http://dx.doi.org/10.1371/journal.pone.0228414
Volume 15
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