Cargando…

Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc

BACKGROUND: Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile benthic dw...

Descripción completa

Detalles Bibliográficos
Autores principales: Wanamaker, Shelly A., Mitchell, Kaitlyn R., Thompson, Rhonda Elliott, Eudeline, Benoit, Vadopalas, Brent, Timmins-Schiffman, Emma B., Roberts, Steven B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7574277/
https://www.ncbi.nlm.nih.gov/pubmed/33076839
http://dx.doi.org/10.1186/s12864-020-07127-3
_version_ 1783597607943143424
author Wanamaker, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Eudeline, Benoit
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
author_facet Wanamaker, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Eudeline, Benoit
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
author_sort Wanamaker, Shelly A.
collection PubMed
description BACKGROUND: Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile benthic dweller while proliferating in environments with broad temperature ranges. Despite the economic and ecological importance of the species, physiological processes occurring throughout metamorphosis and the impact of temperature on these processes have not yet been mapped out. RESULTS: Towards this, we comprehensively characterized protein abundance patterns for 7978 proteins throughout metamorphosis in the Pacific oyster at different temperature regimes. We used a multi-statistical approach including principal component analysis, ANOVA-simultaneous component analysis, and hierarchical clustering coupled with functional enrichment analysis to characterize these data. We identified distinct sets of proteins with time-dependent abundances generally not affected by temperature. Over 12 days, adhesion and calcification related proteins acutely decreased, organogenesis and extracellular matrix related proteins gradually decreased, proteins related to signaling showed sinusoidal abundance patterns, and proteins related to metabolic and growth processes gradually increased. Contrastingly, different sets of proteins showed temperature-dependent abundance patterns with proteins related to immune response showing lower abundance and catabolic pro-growth processes showing higher abundance in animals reared at 29 °C relative to 23 °C. CONCLUSION: Although time was a stronger driver than temperature of metamorphic proteome changes, temperature-induced proteome differences led to pro-growth physiology corresponding to larger oyster size at 29 °C, and to altered specific metamorphic processes and possible pathogen presence at 23 °C. These findings offer high resolution insight into why oysters may experience high mortality rates during this life transition in both field and culture settings. The proteome resource generated by this study provides data-driven guidance for future work on developmental changes in molluscs. Furthermore, the analytical approach taken here provides a foundation for effective shotgun proteomic analyses across a variety of taxa.
format Online
Article
Text
id pubmed-7574277
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-75742772020-10-20 Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc Wanamaker, Shelly A. Mitchell, Kaitlyn R. Thompson, Rhonda Elliott Eudeline, Benoit Vadopalas, Brent Timmins-Schiffman, Emma B. Roberts, Steven B. BMC Genomics Research Article BACKGROUND: Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) undergoes a major phenotypic change in early development from free-swimming larval form to sessile benthic dweller while proliferating in environments with broad temperature ranges. Despite the economic and ecological importance of the species, physiological processes occurring throughout metamorphosis and the impact of temperature on these processes have not yet been mapped out. RESULTS: Towards this, we comprehensively characterized protein abundance patterns for 7978 proteins throughout metamorphosis in the Pacific oyster at different temperature regimes. We used a multi-statistical approach including principal component analysis, ANOVA-simultaneous component analysis, and hierarchical clustering coupled with functional enrichment analysis to characterize these data. We identified distinct sets of proteins with time-dependent abundances generally not affected by temperature. Over 12 days, adhesion and calcification related proteins acutely decreased, organogenesis and extracellular matrix related proteins gradually decreased, proteins related to signaling showed sinusoidal abundance patterns, and proteins related to metabolic and growth processes gradually increased. Contrastingly, different sets of proteins showed temperature-dependent abundance patterns with proteins related to immune response showing lower abundance and catabolic pro-growth processes showing higher abundance in animals reared at 29 °C relative to 23 °C. CONCLUSION: Although time was a stronger driver than temperature of metamorphic proteome changes, temperature-induced proteome differences led to pro-growth physiology corresponding to larger oyster size at 29 °C, and to altered specific metamorphic processes and possible pathogen presence at 23 °C. These findings offer high resolution insight into why oysters may experience high mortality rates during this life transition in both field and culture settings. The proteome resource generated by this study provides data-driven guidance for future work on developmental changes in molluscs. Furthermore, the analytical approach taken here provides a foundation for effective shotgun proteomic analyses across a variety of taxa. BioMed Central 2020-10-19 /pmc/articles/PMC7574277/ /pubmed/33076839 http://dx.doi.org/10.1186/s12864-020-07127-3 Text en © The Author(s) 2020, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wanamaker, Shelly A.
Mitchell, Kaitlyn R.
Thompson, Rhonda Elliott
Eudeline, Benoit
Vadopalas, Brent
Timmins-Schiffman, Emma B.
Roberts, Steven B.
Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_full Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_fullStr Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_full_unstemmed Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_short Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
title_sort temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7574277/
https://www.ncbi.nlm.nih.gov/pubmed/33076839
http://dx.doi.org/10.1186/s12864-020-07127-3
work_keys_str_mv AT wanamakershellya temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT mitchellkaitlynr temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT thompsonrhondaelliott temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT eudelinebenoit temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT vadopalasbrent temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT timminsschiffmanemmab temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc
AT robertsstevenb temporalproteomicprofilingrevealsinsightintocriticaldevelopmentalprocessesandtemperatureinfluencedphysiologicalresponsedifferencesinabivalvemollusc