Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)

Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions. Ausführliche Beschreibung

Gespeichert in:

Autor*in:	Nicolás Zúñiga-Soto [verfasserIn] Ingrid Pinto-Borguero [verfasserIn] Claudio Quevedo [verfasserIn] Felipe Aguilera [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2023

Schlagwörter:	Crassostrea gigas ocean acidification adult oyster secretory cells transcriptome mantle secretome

Übergeordnetes Werk:	In: Frontiers in Marine Science - Frontiers Media S.A., 2015, 10(2023)
Übergeordnetes Werk:	volume:10 ; year:2023

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.3389/fmars.2023.1156831

Katalog-ID:	DOAJ088989488

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spelling	10.3389/fmars.2023.1156831 doi (DE-627)DOAJ088989488 (DE-599)DOAJ4e32e5d93c954bbaa63e7148cf79ffcf DE-627 ger DE-627 rakwb eng QH1-199.5 Nicolás Zúñiga-Soto verfasserin aut Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas) 2023 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions. Crassostrea gigas ocean acidification adult oyster secretory cells transcriptome mantle secretome Science Q General. Including nature conservation, geographical distribution Nicolás Zúñiga-Soto verfasserin aut Ingrid Pinto-Borguero verfasserin aut Ingrid Pinto-Borguero verfasserin aut Claudio Quevedo verfasserin aut Claudio Quevedo verfasserin aut Felipe Aguilera verfasserin aut Felipe Aguilera verfasserin aut In Frontiers in Marine Science Frontiers Media S.A., 2015 10(2023) (DE-627)779393945 (DE-600)2757748-X 22967745 nnns volume:10 year:2023 https://doi.org/10.3389/fmars.2023.1156831 kostenfrei https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf kostenfrei https://www.frontiersin.org/articles/10.3389/fmars.2023.1156831/full kostenfrei https://doaj.org/toc/2296-7745 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_370 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2023
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allfieldsGer	10.3389/fmars.2023.1156831 doi (DE-627)DOAJ088989488 (DE-599)DOAJ4e32e5d93c954bbaa63e7148cf79ffcf DE-627 ger DE-627 rakwb eng QH1-199.5 Nicolás Zúñiga-Soto verfasserin aut Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas) 2023 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions. Crassostrea gigas ocean acidification adult oyster secretory cells transcriptome mantle secretome Science Q General. Including nature conservation, geographical distribution Nicolás Zúñiga-Soto verfasserin aut Ingrid Pinto-Borguero verfasserin aut Ingrid Pinto-Borguero verfasserin aut Claudio Quevedo verfasserin aut Claudio Quevedo verfasserin aut Felipe Aguilera verfasserin aut Felipe Aguilera verfasserin aut In Frontiers in Marine Science Frontiers Media S.A., 2015 10(2023) (DE-627)779393945 (DE-600)2757748-X 22967745 nnns volume:10 year:2023 https://doi.org/10.3389/fmars.2023.1156831 kostenfrei https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf kostenfrei https://www.frontiersin.org/articles/10.3389/fmars.2023.1156831/full kostenfrei https://doaj.org/toc/2296-7745 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_370 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 10 2023
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topic_title	QH1-199.5 Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas) Crassostrea gigas ocean acidification adult oyster secretory cells transcriptome mantle secretome
topic	misc QH1-199.5 misc Crassostrea gigas misc ocean acidification misc adult oyster misc secretory cells misc transcriptome misc mantle secretome misc Science misc Q misc General. Including nature conservation, geographical distribution
topic_unstemmed	misc QH1-199.5 misc Crassostrea gigas misc ocean acidification misc adult oyster misc secretory cells misc transcriptome misc mantle secretome misc Science misc Q misc General. Including nature conservation, geographical distribution
topic_browse	misc QH1-199.5 misc Crassostrea gigas misc ocean acidification misc adult oyster misc secretory cells misc transcriptome misc mantle secretome misc Science misc Q misc General. Including nature conservation, geographical distribution
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title	Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
ctrlnum	(DE-627)DOAJ088989488 (DE-599)DOAJ4e32e5d93c954bbaa63e7148cf79ffcf
title_full	Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
author_sort	Nicolás Zúñiga-Soto
journal	Frontiers in Marine Science
journalStr	Frontiers in Marine Science
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lang_code	eng
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author_browse	Nicolás Zúñiga-Soto Ingrid Pinto-Borguero Claudio Quevedo Felipe Aguilera
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author-letter	Nicolás Zúñiga-Soto
doi_str_mv	10.3389/fmars.2023.1156831
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title_sort	secretory and transcriptomic responses of mantle cells to low ph in the pacific oyster (crassostrea gigas)
callnumber	QH1-199.5
title_auth	Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
abstract	Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions.
abstractGer	Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions.
abstract_unstemmed	Since the Industrial Revolution, the concentration of atmospheric carbon dioxide (CO2) due to anthropogenic activities has increased at unprecedented rates. One-third of the atmospheric anthropogenic CO2 emissions are dissolved in the oceans affecting the chemical equilibrium of seawater, which in turn leads to a decrease in pH and carbonate ion (CO32-) concentration, a phenomenon known as ocean acidification (OA). This chemical disequilibrium can be detrimental to marine organisms (e.g., mollusks) that fabricate mineralized structures based on calcium carbonate (CaCO3). Most studies on the effect of reduced pH in seawater have been conducted on the early developmental stages of shell-building invertebrates, given less attention to how adult individuals face OA stress. Here, we evaluate histological, secretory, and transcriptional changes in the mantle of adult oysters (Crassostrea gigas) exposure to ambient (8.0 ± 0.2) and reduced (7.6 ± 0.2) pH during 20 days. Most histological observations did not show differences in terms of mantle cell morphology. However, Alcian Blue/PAS staining revealed significant differences in the number of Alcian Blue positive cells in the mantle edge, suggesting a decrease in the secretory activity in this morphogenetic zone. Transcriptomic analysis revealed 172 differentially expressed genes (DEGs) between mantle tissues from adult oysters kept in normal and reduced pH conditions. Almost 18% of the DEGs encode secreted proteins that are likely to be contributing to shell fabrication and patterning. 17 of 31 DEGs encoding secreted proteins correspond to oyster-specific genes, highlighting the fact that molluscan shell formation is underpinned by a rapidly evolving secretome. The GO analysis of DEGs encoding secreted proteins showed that they are involved in the cellular response to stimulus, response to stress, protein binding, and ion binding, suggesting these biological processes and molecular functions are altered by OA. This study demonstrates that histology and gene expression profiling can advance our understanding of the cellular and molecular mechanisms underlying adult oyster tolerance to low pH conditions.
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title_short	Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
url	https://doi.org/10.3389/fmars.2023.1156831 https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf https://www.frontiersin.org/articles/10.3389/fmars.2023.1156831/full https://doaj.org/toc/2296-7745
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author2	Nicolás Zúñiga-Soto Ingrid Pinto-Borguero Claudio Quevedo Felipe Aguilera
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up_date	2024-07-03T20:37:02.579Z
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Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)

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