Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails

Handle URI:
http://hdl.handle.net/10754/626132
Title:
Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails
Authors:
Mu, Huawei; Sun, Jin; Cheung, Siu Gin; Fang, Ling; Zhou, Haiyun; Luan, Tiangang; Zhang, Huoming ( 0000-0001-5416-0358 ) ; Wong, Chris K.C.; Qiu, Jian-Wen ( 0000-0002-1541-9627 )
Abstract:
Although high-throughput proteomics has been widely applied to study mechanisms of environmental adaptation, the conclusions from studies that are based on one species can be confounded by phylogeny. We compare the freshwater snail Pomacea canaliculata (a notorious invasive species) and its congener Pomacea diffusa (a non-invasive species) to understand the molecular mechanisms of their differential resistance to hypoxia. A 72-h acute exposure experiment showed that P. canaliculata is more tolerant to hypoxia than P. diffusa. The two species were then exposed to three levels of dissolved oxygen (6.7, 2.0 and 1.0mgL−1) for 8h, and their gill proteins were analyzed using iTRAQ-coupled LC-MS/MS. The two species showed striking differences in protein expression profiles, with the more hypoxia tolerant P. canaliculata having more up-regulated proteins in signal transduction and down-regulated proteins in glycolysis and the tricarboxylic acid cycle. Evolutionary analysis revealed five orthologous genes encoding differentially expressed proteins having clear signal of positive selection, indicating selection has acted on some of the hypoxia responsive genes. Our case study has highlighted the potential of integrated proteomics and comparative evolutionary analysis for understanding the genetic basis of adaptation to global environmental change in non-model species. SignificanceRapid globalization in recent decades has greatly facilitated species introduction around the world. Successfully established introduced species, so-called invasive species, have threatened the invaded ecosystems. There has been substantial interest in studying how invasive species respond to extreme environmental conditions because the results can help not only predict their range of expansion and manage their impact, but also may reveal the adaptive mechanisms underlying their invasiveness. Our study has adopted a comparative approach to study the differential physiological and proteomic responses of two congeneric snails to various hypoxic conditions, as well as codon substitution analysis at transcriptomic level to detect signals of positive selection in hypoxia-responsive genes. The integrated physiological, proteomic and transcriptomic approach can be applied in other non-model species to understand the molecular mechanisms of adaptation to global environmental change.
KAUST Department:
Biosciences Core Lab
Citation:
Mu H, Sun J, Cheung SG, Fang L, Zhou H, et al. (2017) Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails. Journal of Proteomics. Available: http://dx.doi.org/10.1016/j.jprot.2017.11.002.
Publisher:
Elsevier BV
Journal:
Journal of Proteomics
Issue Date:
6-Nov-2017
DOI:
10.1016/j.jprot.2017.11.002
Type:
Article
ISSN:
1874-3919
Sponsors:
This work was supported by the General Research Fund of Hong Kong (grant no.HKBU261312 and HKBU12301415) and Hong Kong Baptist University (grant no.SDF 15-1012-P04). We thank Dr. Brent L. Lockwood for providing an R script for ANOVA, Dr. Runsheng Li for advice on statistical analysis, and Ms. Haoyu Zhang for assistance in setting up the hypoxia exposure system.
Additional Links:
http://www.sciencedirect.com/science/article/pii/S187439191730372X
Appears in Collections:
Articles; Bioscience Core Lab

Full metadata record

DC FieldValue Language
dc.contributor.authorMu, Huaweien
dc.contributor.authorSun, Jinen
dc.contributor.authorCheung, Siu Ginen
dc.contributor.authorFang, Lingen
dc.contributor.authorZhou, Haiyunen
dc.contributor.authorLuan, Tiangangen
dc.contributor.authorZhang, Huomingen
dc.contributor.authorWong, Chris K.C.en
dc.contributor.authorQiu, Jian-Wenen
dc.date.accessioned2017-11-09T06:33:07Z-
dc.date.available2017-11-09T06:33:07Z-
dc.date.issued2017-11-06en
dc.identifier.citationMu H, Sun J, Cheung SG, Fang L, Zhou H, et al. (2017) Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails. Journal of Proteomics. Available: http://dx.doi.org/10.1016/j.jprot.2017.11.002.en
dc.identifier.issn1874-3919en
dc.identifier.doi10.1016/j.jprot.2017.11.002en
dc.identifier.urihttp://hdl.handle.net/10754/626132-
dc.description.abstractAlthough high-throughput proteomics has been widely applied to study mechanisms of environmental adaptation, the conclusions from studies that are based on one species can be confounded by phylogeny. We compare the freshwater snail Pomacea canaliculata (a notorious invasive species) and its congener Pomacea diffusa (a non-invasive species) to understand the molecular mechanisms of their differential resistance to hypoxia. A 72-h acute exposure experiment showed that P. canaliculata is more tolerant to hypoxia than P. diffusa. The two species were then exposed to three levels of dissolved oxygen (6.7, 2.0 and 1.0mgL−1) for 8h, and their gill proteins were analyzed using iTRAQ-coupled LC-MS/MS. The two species showed striking differences in protein expression profiles, with the more hypoxia tolerant P. canaliculata having more up-regulated proteins in signal transduction and down-regulated proteins in glycolysis and the tricarboxylic acid cycle. Evolutionary analysis revealed five orthologous genes encoding differentially expressed proteins having clear signal of positive selection, indicating selection has acted on some of the hypoxia responsive genes. Our case study has highlighted the potential of integrated proteomics and comparative evolutionary analysis for understanding the genetic basis of adaptation to global environmental change in non-model species. SignificanceRapid globalization in recent decades has greatly facilitated species introduction around the world. Successfully established introduced species, so-called invasive species, have threatened the invaded ecosystems. There has been substantial interest in studying how invasive species respond to extreme environmental conditions because the results can help not only predict their range of expansion and manage their impact, but also may reveal the adaptive mechanisms underlying their invasiveness. Our study has adopted a comparative approach to study the differential physiological and proteomic responses of two congeneric snails to various hypoxic conditions, as well as codon substitution analysis at transcriptomic level to detect signals of positive selection in hypoxia-responsive genes. The integrated physiological, proteomic and transcriptomic approach can be applied in other non-model species to understand the molecular mechanisms of adaptation to global environmental change.en
dc.description.sponsorshipThis work was supported by the General Research Fund of Hong Kong (grant no.HKBU261312 and HKBU12301415) and Hong Kong Baptist University (grant no.SDF 15-1012-P04). We thank Dr. Brent L. Lockwood for providing an R script for ANOVA, Dr. Runsheng Li for advice on statistical analysis, and Ms. Haoyu Zhang for assistance in setting up the hypoxia exposure system.en
dc.publisherElsevier BVen
dc.relation.urlhttp://www.sciencedirect.com/science/article/pii/S187439191730372Xen
dc.rightsNOTICE: this is the author’s version of a work that was accepted for publication in Journal of Proteomics. Changes resulting from the publishing process, such as peer review, editing, corrections, structural formatting, and other quality control mechanisms may not be reflected in this document. Changes may have been made to this work since it was submitted for publication. A definitive version was subsequently published in Journal of Proteomics, [, , (2017-11-06)] DOI: 10.1016/j.jprot.2017.11.002 . © 2017. This manuscript version is made available under the CC-BY-NC-ND 4.0 license http://creativecommons.org/licenses/by-nc-nd/4.0/en
dc.subjectStress responseen
dc.subjectInvasive speciesen
dc.subjectPomaceaen
dc.subjectProteomicsen
dc.subjectEpigeneticsen
dc.titleComparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snailsen
dc.typeArticleen
dc.contributor.departmentBiosciences Core Laben
dc.identifier.journalJournal of Proteomicsen
dc.eprint.versionPost-printen
dc.contributor.institutionDepartment of Biology, Hong Kong Baptist University, Hong Kong, Chinaen
dc.contributor.institutionDivision of Life Science, The Hong Kong University of Science and Technology, Hong Kong, Chinaen
dc.contributor.institutionDepartment of Biology and Chemistry, City University of Hong Kong, Hong Kong, Chinaen
dc.contributor.institutionInstrumental Analysis and Research Center, Sun Yat-Sen University, Guangzhou, PR Chinaen
dc.contributor.institutionMOE Key Laboratory of Aquatic Product Safety, School of Life Sciences, Sun Yat-Sen University, Guangzhou, PR Chinaen
kaust.authorZhang, Huomingen
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