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 t...

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Published in:Frontiers in Marine Science
Main Authors: Nicolás Zúñiga-Soto, Ingrid Pinto-Borguero, Claudio Quevedo, Felipe Aguilera
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2023
Subjects:
Q
Online Access:https://doi.org/10.3389/fmars.2023.1156831
https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf
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spelling ftdoajarticles:oai:doaj.org/article:4e32e5d93c954bbaa63e7148cf79ffcf 2023-06-06T11:52:56+02:00 Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas) Nicolás Zúñiga-Soto Ingrid Pinto-Borguero Claudio Quevedo Felipe Aguilera 2023-04-01T00:00:00Z https://doi.org/10.3389/fmars.2023.1156831 https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fmars.2023.1156831/full https://doaj.org/toc/2296-7745 2296-7745 doi:10.3389/fmars.2023.1156831 https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf Frontiers in Marine Science, Vol 10 (2023) Crassostrea gigas ocean acidification adult oyster secretory cells transcriptome mantle secretome Science Q General. Including nature conservation geographical distribution QH1-199.5 article 2023 ftdoajarticles https://doi.org/10.3389/fmars.2023.1156831 2023-04-16T00:38:08Z 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 ... Article in Journal/Newspaper Crassostrea gigas Ocean acidification Pacific oyster Directory of Open Access Journals: DOAJ Articles Pacific Frontiers in Marine Science 10
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Crassostrea gigas
ocean acidification
adult oyster
secretory cells
transcriptome
mantle secretome
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
spellingShingle Crassostrea gigas
ocean acidification
adult oyster
secretory cells
transcriptome
mantle secretome
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
Nicolás Zúñiga-Soto
Ingrid Pinto-Borguero
Claudio Quevedo
Felipe Aguilera
Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
topic_facet Crassostrea gigas
ocean acidification
adult oyster
secretory cells
transcriptome
mantle secretome
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
description 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 ...
format Article in Journal/Newspaper
author Nicolás Zúñiga-Soto
Ingrid Pinto-Borguero
Claudio Quevedo
Felipe Aguilera
author_facet Nicolás Zúñiga-Soto
Ingrid Pinto-Borguero
Claudio Quevedo
Felipe Aguilera
author_sort Nicolás Zúñiga-Soto
title Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
title_short Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
title_full Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
title_fullStr Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
title_full_unstemmed Secretory and transcriptomic responses of mantle cells to low pH in the Pacific oyster (Crassostrea gigas)
title_sort secretory and transcriptomic responses of mantle cells to low ph in the pacific oyster (crassostrea gigas)
publisher Frontiers Media S.A.
publishDate 2023
url https://doi.org/10.3389/fmars.2023.1156831
https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Ocean acidification
Pacific oyster
genre_facet Crassostrea gigas
Ocean acidification
Pacific oyster
op_source Frontiers in Marine Science, Vol 10 (2023)
op_relation https://www.frontiersin.org/articles/10.3389/fmars.2023.1156831/full
https://doaj.org/toc/2296-7745
2296-7745
doi:10.3389/fmars.2023.1156831
https://doaj.org/article/4e32e5d93c954bbaa63e7148cf79ffcf
op_doi https://doi.org/10.3389/fmars.2023.1156831
container_title Frontiers in Marine Science
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