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Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus.

ABSTRACT: BACKGROUND: The Mozambique tilapia Oreochromis mossambicus has the ability to adapt to a broad range of environmental salinities and has long been used for investigating iono-osmoregulation. However, to date most studies have focused mainly on several key molecules or parameters hence yielding a limited perspective of the versatile iono-osmoregulation in the euryhaline fish. This study aimed to capture transcriptome-wide differences between the freshwater- and seawater-acclimated gills of the Mozambique tilapia. RESULTS: We have identified over 5000 annotated gene transcripts with high homology (E-value <1.0E-50) to human genes that were differentially expressed in freshwater- and seawater-acclimated gills of the Mozambique tilapia. These putative human homologs were found to be significantly associated with over 50 canonical signaling pathways that are operating in at least 23 biological processes in relation to branchial iono-osmoregulation and cellular remodeling. The analysis revealed multiple signaling pathways in freshwater-acclimated gills acting in concert to maintain cellular homeostasis under hypo-osmotic environment while seawater-acclimated gills abounded with molecular signals to cope with the higher cellular turn-over rate, energetics and iono-regulatory demands under hyper-osmostic stress. Additionally, over 100 transcripts encoding putative inorganic ion transporters/channels were identified, of which several are well established in gill iono-regulation while the remainder are lesser known. We have also validated the expression profiles of 47 representative genes in freshwater- and seawater-acclimated gills, as well as in hypersaline-acclimated (two-fold salinity of seawater) gills. The findings confirmed that many of these responsive genes retained their expression profiles in hypersaline-acclimated gills as in seawater-acclimated gills, although several genes had changed significantly in their expression level/direction in hypersaline-acclimated gills. CONCLUSIONS: This is the first study that has provided an unprecedented transcriptomic-wide perspective of gill iono-osmoregulation since such studies were initiated more than 80 years ago. It has expanded our molecular perspective from a relatively few well-studied molecules to a plethora of gene transcripts and a myriad of canonical signaling pathways driving various biological processes that are operating in gills under hypo-osmotic and hyper-osmotic stresses. These findings would provide insights and resources to fuel future studies on gill iono-osmoregulation and cellular remodeling in response to salinity challenge and acclimation.

SUBMITTER: Lam SH

PROVIDER: S-EPMC4213501 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus.

Lam Siew Hong SH Lui Eei Yin EY Li Zhengjun Z Cai Shaojiang S Sung Wing-Kin WK Mathavan Sinnakaruppan S Lam Toong Jin TJ Ip Yuen Kwong YK

BMC genomics 20141023

<h4>Background</h4>The Mozambique tilapia Oreochromis mossambicus has the ability to adapt to a broad range of environmental salinities and has long been used for investigating iono-osmoregulation. However, to date most studies have focused mainly on several key molecules or parameters hence yielding a limited perspective of the versatile iono-osmoregulation in the euryhaline fish. This study aimed to capture transcriptome-wide differences between the freshwater- and seawater-acclimated gills of ...[more]

PMID: 25342237

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Project description:BACKGROUND:Osmotic stress is a widespread phenomenon in aquatic animal. The ability to cope with salinity stress and alkaline stress is quite important for the survival of aquatic species under natural conditions. Tilapia is an important commercial euryhaline fish species. What's more tilapia is a good experimental material for osmotic stress regulation research, but the molecular regulation mechanism underlying different osmotic pressure of tilapia is still unexplored. RESULTS:To elucidate the osmoregulation strategy behind its hyper salinity, alkalinity and salinity-alkalinity stress of tilapia, the transcriptomes of gills in hybrid tilapia (Oreochromis mossambicus ??×?O. urolepis hornorum ?) under salinity stress (S: 25‰), alkalinity stress(A: 4‰) and salinity-alkalinity stress (SA: S: 15‰, A: 4‰) were sequenced using deep-sequencing platform Illumina/HiSeq-2000 and differential expression genes (DEGs) were identified. A total of 1958, 1472 and 1315 upregulated and 1824, 1940 and 1735 downregulated genes (P-value <?0.05) were identified in the salt stress, alkali stress and saline-alkali stress groups, respectively, compared with those in the control group. Furthermore, Kyoto Encyclopedia of Genes and Genomes pathway analyses were conducted in the significant different expression genes. In all significant DEGs, some of the typical genes involved in osmoregulation, including carbonic anhydrase (CA), calcium/calmodulin-dependent protein kinase (CaM kinase) II (CAMK2), aquaporin-1(AQP1), sodium bicarbonate cotransporter (SLC4A4/NBC1), chloride channel 2(CLCN2), sodium/potassium/chloride transporter (SLC12A2 / NKCC1) and other osmoregulation genes were also identified. RNA-seq results were validated with quantitative real-time PCR (qPCR), the 17 random selected genes showed a consistent direction in both RNA-Seq and qPCR analysis, demonstrated that the results of RNA-seq were reliable. CONCLUSIONS:The present results would be helpful to elucidate the osmoregulation mechanism of aquatic animals adapting to saline-alkali challenge. This study provides a global overview of gene expression patterns and pathways that related to osmoregulation in hybrid tilapia, and could contribute to a better understanding of the molecular regulation mechanism in different osmotic stresses.

Project description:The ability of euryhaline Mozambique tilapia to tolerate extreme environmental salinities makes it an excellent model for investigating iono-regulation. This study aimed to characterize and fill important information gap of the expression levels of key ion transporters for Na(+) and Cl(-) in the gill and esophageal-gastrointestinal tract of Mozambique tilapia acclimated to freshwater (0 ppt), seawater (30 ppt) and hypersaline (70 ppt) environments. Among the seven genes studied, it was found that nkcc2, nkcc1a, cftr, nka-α1 and nka-α3, were more responsive to salinity challenge than nkcc1b and ncc within the investigated tissues. The ncc expression was restricted to gills of freshwater-acclimated fish while nkcc2 expression was restricted to intestinal segments irrespective of salinity challenge. Among the tissues investigated, gill and posterior intestine were found to be highly responsive to salinity changes, followed by anterior and middle intestine. Both esophagus and stomach displayed significant up-regulation of nka-α1 and nka-α3, but not nkcc isoforms and cftr, in hypersaline-acclimated fish suggesting a response to hypersalinity challenge and involvement of other forms of transporters in iono-regulation. Changes in gene expression levels were partly corroborated by immunohistochemical localization of transport proteins. Apical expression of Ncc was found in Nka-immunoreactive cells in freshwater-acclimated gills while Nkcc co-localized with Nka-immunoreactive cells expressing Cftr apically in seawater- and hypersaline-acclimated gills. In the intestine, Nkcc-stained apical brush border was found in Nka-immunoreactive cells at greater levels under hypersaline conditions. These findings provided new insights into the responsiveness of these genes and tissues under hypersalinity challenge, specifically the posterior intestine being vital for salt absorption and iono-osmoregulation in the Mozambique tilapia; its ability to survive in hypersalinity may be in part related to its ability to up-regulate key ion transporters in the posterior intestine. The findings pave the way for future iono-regulatory studies on the Mozambique tilapia esophageal-gastrointestinal tract.

Dataset Information

Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus.

Publications

Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus.

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