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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Published in:Oceans
Main Authors: Marleen Stuhr, Louise P. Cameron, Bernhard Blank-Landeshammer, Claire E. Reymond, Steve S. Doo, Hildegard Westphal, Albert Sickmann, Justin B. Ries
Format: Text
Language:English
Published: Multidisciplinary Digital Publishing Institute 2021
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Online Access:https://doi.org/10.3390/oceans2020017
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spelling ftmdpi:oai:mdpi.com:/2673-1924/2/2/17/ 2023-08-20T04:08:58+02:00 Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios Marleen Stuhr Louise P. Cameron Bernhard Blank-Landeshammer Claire E. Reymond Steve S. Doo Hildegard Westphal Albert Sickmann Justin B. Ries agris 2021-04-01 application/pdf https://doi.org/10.3390/oceans2020017 EN eng Multidisciplinary Digital Publishing Institute https://dx.doi.org/10.3390/oceans2020017 https://creativecommons.org/licenses/by/4.0/ Oceans; Volume 2; Issue 2; Pages: 281-314 Amphistegina lobifera coral reef global warming large benthic foraminifera LC-MS/MS proteomics ocean acidification pH microsensor photosymbiotic calcifier Red Sea thermal stress Text 2021 ftmdpi https://doi.org/10.3390/oceans2020017 2023-08-01T01:25:02Z 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, Amphistegina lobifera from the Gulf of Aqaba were cultured under three pCO2 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 pCO2 caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing pCO2 under all light/dark and temperature combinations. However, the difference between [H+] at the test surface and [H+] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and pCO2. 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-pCO2 and 31 °C and putative decreases in test stability at high-pCO2 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. Text Ocean acidification MDPI Open Access Publishing Oceans 2 2 281 314
institution Open Polar
collection MDPI Open Access Publishing
op_collection_id ftmdpi
language English
topic Amphistegina lobifera
coral reef
global warming
large benthic foraminifera
LC-MS/MS proteomics
ocean acidification
pH microsensor
photosymbiotic calcifier
Red Sea
thermal stress
spellingShingle Amphistegina lobifera
coral reef
global warming
large benthic foraminifera
LC-MS/MS proteomics
ocean acidification
pH microsensor
photosymbiotic calcifier
Red Sea
thermal stress
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
topic_facet Amphistegina lobifera
coral reef
global warming
large benthic foraminifera
LC-MS/MS proteomics
ocean acidification
pH microsensor
photosymbiotic calcifier
Red Sea
thermal stress
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, Amphistegina lobifera from the Gulf of Aqaba were cultured under three pCO2 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 pCO2 caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing pCO2 under all light/dark and temperature combinations. However, the difference between [H+] at the test surface and [H+] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and pCO2. 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-pCO2 and 31 °C and putative decreases in test stability at high-pCO2 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.
format Text
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
title 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_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_sort divergent proteomic responses offer insights into resistant physiological responses of a reef-foraminifera to climate change scenarios
publisher Multidisciplinary Digital Publishing Institute
publishDate 2021
url https://doi.org/10.3390/oceans2020017
op_coverage agris
genre Ocean acidification
genre_facet Ocean acidification
op_source Oceans; Volume 2; Issue 2; Pages: 281-314
op_relation https://dx.doi.org/10.3390/oceans2020017
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3390/oceans2020017
container_title Oceans
container_volume 2
container_issue 2
container_start_page 281
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