Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios

Reef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive to climate change. To gain insight into th...

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Main Authors: Marleen Stuhr, Louise P. Cameron, Bernhard Blank-Landeshammer, Claire E. Reymond, Steve S. Doo, Hildegard Westphal, Albert Sickmann, Justin B. Ries
Format: Article
Language:English
Published: MDPI AG 2021-04-01
Series:Oceans
Subjects:
Online Access:https://www.mdpi.com/2673-1924/2/2/17
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author Marleen Stuhr
Louise P. Cameron
Bernhard Blank-Landeshammer
Claire E. Reymond
Steve S. Doo
Hildegard Westphal
Albert Sickmann
Justin B. Ries
author_facet Marleen Stuhr
Louise P. Cameron
Bernhard Blank-Landeshammer
Claire E. Reymond
Steve S. Doo
Hildegard Westphal
Albert Sickmann
Justin B. Ries
author_sort Marleen Stuhr
collection DOAJ
description Reef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive to climate change. To gain insight into their responses to near-future conditions, <i>Amphistegina lobifera</i> from the Gulf of Aqaba were cultured under three <i>p</i>CO<sub>2</sub> conditions (492, 963, 3182 ppm) crossed with two temperature conditions (28 °C, 31 °C) for two months. Differential protein abundances in host and photosymbionts were investigated alongside physiological responses and microenvironmental pH gradients assessed via proton microsensors. Over 1000 proteins were identified, of which > 15% varied significantly between treatments. Thermal stress predominantly reduced protein abundances, and holobiont growth. Elevated <i>p</i>CO<sub>2</sub> caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing <i>p</i>CO<sub>2</sub> under all light/dark and temperature combinations. However, the difference between [H<sup>+</sup>] at the test surface and [H<sup>+</sup>] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and <i>p</i>CO<sub>2</sub>. Combined stressors resulted in reduced pore sizes and increased microenvironmental pH gradients, indicating acclimative mechanisms that support calcite test production and/or preservation under climate change. Substantial proteomic variations at moderate-<i>p</i>CO<sub>2</sub> and 31 °C and putative decreases in test stability at high-<i>p</i>CO<sub>2</sub> and 31 °C indicate cellular modifications and impacts on calcification, in contrast to the LBFs’ apparently stable overall physiological performance. Our experiment shows that the effects of climate change can be missed when stressors are assessed in isolation, and that physiological responses should be assessed across organismal levels to make more meaningful inferences about the fate of reef calcifiers.
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spelling doaj.art-43349237d6e2425ab20e7bd6b44a7f4a2023-11-21T13:52:36ZengMDPI AGOceans2673-19242021-04-012228131410.3390/oceans2020017Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change ScenariosMarleen Stuhr0Louise P. Cameron1Bernhard Blank-Landeshammer2Claire E. Reymond3Steve S. Doo4Hildegard Westphal5Albert Sickmann6Justin B. Ries7Interuniversity Institute for Marine Sciences, Eilat 8810302, IsraelLeibniz Centre for Tropical Marine Research (ZMT), 28359 Bremen, GermanyLeibniz Institut für Analytische Wissenschaften-ISAS-e.V., 44139 Dortmund, GermanyLeibniz Centre for Tropical Marine Research (ZMT), 28359 Bremen, GermanyLeibniz Centre for Tropical Marine Research (ZMT), 28359 Bremen, GermanyLeibniz Centre for Tropical Marine Research (ZMT), 28359 Bremen, GermanyLeibniz Institut für Analytische Wissenschaften-ISAS-e.V., 44139 Dortmund, GermanyLeibniz Centre for Tropical Marine Research (ZMT), 28359 Bremen, GermanyReef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive to climate change. To gain insight into their responses to near-future conditions, <i>Amphistegina lobifera</i> from the Gulf of Aqaba were cultured under three <i>p</i>CO<sub>2</sub> conditions (492, 963, 3182 ppm) crossed with two temperature conditions (28 °C, 31 °C) for two months. Differential protein abundances in host and photosymbionts were investigated alongside physiological responses and microenvironmental pH gradients assessed via proton microsensors. Over 1000 proteins were identified, of which > 15% varied significantly between treatments. Thermal stress predominantly reduced protein abundances, and holobiont growth. Elevated <i>p</i>CO<sub>2</sub> caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing <i>p</i>CO<sub>2</sub> under all light/dark and temperature combinations. However, the difference between [H<sup>+</sup>] at the test surface and [H<sup>+</sup>] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and <i>p</i>CO<sub>2</sub>. Combined stressors resulted in reduced pore sizes and increased microenvironmental pH gradients, indicating acclimative mechanisms that support calcite test production and/or preservation under climate change. Substantial proteomic variations at moderate-<i>p</i>CO<sub>2</sub> and 31 °C and putative decreases in test stability at high-<i>p</i>CO<sub>2</sub> and 31 °C indicate cellular modifications and impacts on calcification, in contrast to the LBFs’ apparently stable overall physiological performance. Our experiment shows that the effects of climate change can be missed when stressors are assessed in isolation, and that physiological responses should be assessed across organismal levels to make more meaningful inferences about the fate of reef calcifiers.https://www.mdpi.com/2673-1924/2/2/17<i>Amphistegina lobifera</i>coral reefglobal warminglarge benthic foraminiferaLC-MS/MS proteomicsocean acidification
spellingShingle Marleen Stuhr
Louise P. Cameron
Bernhard Blank-Landeshammer
Claire E. Reymond
Steve S. Doo
Hildegard Westphal
Albert Sickmann
Justin B. Ries
Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
Oceans
<i>Amphistegina lobifera</i>
coral reef
global warming
large benthic foraminifera
LC-MS/MS proteomics
ocean acidification
title Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
title_full Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
title_fullStr Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
title_full_unstemmed Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
title_short Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
title_sort divergent proteomic responses offer insights into resistant physiological responses of a reef foraminifera to climate change scenarios
topic <i>Amphistegina lobifera</i>
coral reef
global warming
large benthic foraminifera
LC-MS/MS proteomics
ocean acidification
url https://www.mdpi.com/2673-1924/2/2/17
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