Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure

We recently demonstrated the rapid adaptation of Red Sea phytoplankton to ocean warming, with associated constraints on physiological performance. However, the possible tradeoff between thermal adaptation and the organism's tolerance to other environmental drivers in a warmer future remains und...

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Main Authors: Sreejith Kottuparambil, Peng Jin, Susana Agusti
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Environmental Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fenvs.2019.00125/full
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author Sreejith Kottuparambil
Peng Jin
Peng Jin
Susana Agusti
author_facet Sreejith Kottuparambil
Peng Jin
Peng Jin
Susana Agusti
author_sort Sreejith Kottuparambil
collection DOAJ
description We recently demonstrated the rapid adaptation of Red Sea phytoplankton to ocean warming, with associated constraints on physiological performance. However, the possible tradeoff between thermal adaptation and the organism's tolerance to other environmental drivers in a warmer future remains understudied. Here, we designed an evolutionary selection environment where the Red Sea diatom Chaetoceros tenuissimus was adapted to ambient (26°C) and warming (30°C) temperature scenarios for over 2,000 generations. These strains were subsequently exposed to a range of copper (Cu) dose over three assay temperatures (26, 30, and 35°C), to assess whether adaptation to experimental warming is accompanied by a reformed tolerance to toxic pollutants. Most previous studies on Cu toxicity in marine phytoplankton were conducted within a smaller range of temperature (20–25°C), indicating the need for further assessments to reveal the potential complex interactive effects between pollutants and more significant warming in the future. The acute Cu toxicity was estimated in terms of reduction in cell abundance (cells mL−1), growth rate (μ) and PSII photosynthetic efficiency (Fv/Fm), with 48 h median effective concentration values (EC50) ranging from 2.22 to 20.19 μg L−1. We found a statistically significant interaction between assay temperature, selection temperature, and Cu doses in all the criteria tested. However, under the extreme warming scenario (35°C), the Cu sensitivity was significantly reduced, indicating cumulative antagonistic effects between these factors. Adaptation of phytoplankton to higher temperatures may help maintain their heavy metal tolerance, although a shift in temperature during the tests clearly altered their sensitivities. We conclude that selection for warming had made cells more resistant to Cu at the selection temperature in comparison to ambient-adapted population tested at 26°C. However, in warming-adapted cells, this response was traded off against cupper resistance at 26°C.
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spelling doaj.art-a397fb95939d4c47a793c20404b4eb162022-12-22T00:30:44ZengFrontiers Media S.A.Frontiers in Environmental Science2296-665X2019-08-01710.3389/fenvs.2019.00125470385Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal ExposureSreejith Kottuparambil0Peng Jin1Peng Jin2Susana Agusti3Division of Biological and Environmental Science and Engineering (BESE), Red Sea Research Center (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDivision of Biological and Environmental Science and Engineering (BESE), Red Sea Research Center (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaSchool of Environmental Science and Engineering, Guangzhou University, Guangzhou, ChinaDivision of Biological and Environmental Science and Engineering (BESE), Red Sea Research Center (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaWe recently demonstrated the rapid adaptation of Red Sea phytoplankton to ocean warming, with associated constraints on physiological performance. However, the possible tradeoff between thermal adaptation and the organism's tolerance to other environmental drivers in a warmer future remains understudied. Here, we designed an evolutionary selection environment where the Red Sea diatom Chaetoceros tenuissimus was adapted to ambient (26°C) and warming (30°C) temperature scenarios for over 2,000 generations. These strains were subsequently exposed to a range of copper (Cu) dose over three assay temperatures (26, 30, and 35°C), to assess whether adaptation to experimental warming is accompanied by a reformed tolerance to toxic pollutants. Most previous studies on Cu toxicity in marine phytoplankton were conducted within a smaller range of temperature (20–25°C), indicating the need for further assessments to reveal the potential complex interactive effects between pollutants and more significant warming in the future. The acute Cu toxicity was estimated in terms of reduction in cell abundance (cells mL−1), growth rate (μ) and PSII photosynthetic efficiency (Fv/Fm), with 48 h median effective concentration values (EC50) ranging from 2.22 to 20.19 μg L−1. We found a statistically significant interaction between assay temperature, selection temperature, and Cu doses in all the criteria tested. However, under the extreme warming scenario (35°C), the Cu sensitivity was significantly reduced, indicating cumulative antagonistic effects between these factors. Adaptation of phytoplankton to higher temperatures may help maintain their heavy metal tolerance, although a shift in temperature during the tests clearly altered their sensitivities. We conclude that selection for warming had made cells more resistant to Cu at the selection temperature in comparison to ambient-adapted population tested at 26°C. However, in warming-adapted cells, this response was traded off against cupper resistance at 26°C.https://www.frontiersin.org/article/10.3389/fenvs.2019.00125/fullRed SeaChaetoceroswarmingadaptationcopper toxicityFv/Fm
spellingShingle Sreejith Kottuparambil
Peng Jin
Peng Jin
Susana Agusti
Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
Frontiers in Environmental Science
Red Sea
Chaetoceros
warming
adaptation
copper toxicity
Fv/Fm
title Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
title_full Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
title_fullStr Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
title_full_unstemmed Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
title_short Adaptation of Red Sea Phytoplankton to Experimental Warming Increases Their Tolerance to Toxic Metal Exposure
title_sort adaptation of red sea phytoplankton to experimental warming increases their tolerance to toxic metal exposure
topic Red Sea
Chaetoceros
warming
adaptation
copper toxicity
Fv/Fm
url https://www.frontiersin.org/article/10.3389/fenvs.2019.00125/full
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AT pengjin adaptationofredseaphytoplanktontoexperimentalwarmingincreasestheirtolerancetotoxicmetalexposure
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