Discovery of osmotic sensitive transcription factors in fish intestine via a transcriptomic approach

Abstract

BackgroundTeleost intestine is crucial for seawater acclimation by sensing osmolality of imbibed seawater and regulating drinking and water/ion absorption. Regulatory genes for transforming intestinal function have not been identified. A transcriptomic approach was used to search for such genes in the intestine of euryhaline medaka.ResultsQuantitative RNA-seq by Illumina Hi-Seq Sequencing method was performed to analyze intestinal gene expression 0 h, 1 h, 3 h, 1 d, and 7 d after seawater transfer. Gene ontology (GO) enrichment results showed that cell adhesion, signal transduction, and protein phosphorylation gene categories were augmented soon after transfer, indicating a rapid reorganization of cellular components and functions. Among >50 transiently up-regulated transcription factors selected via co-expression correlation and GO selection, five transcription factors, including CEBPB and CEBPD, were confirmed by quantitative PCR to be specific to hyperosmotic stress, while others were also up-regulated after freshwater control transfer, including some well-known osmotic-stress transcription factors such as SGK1 and TSC22D3/Ostf1. Protein interaction networks suggest a high degree of overlapping among the signaling of transcription factors that respond to osmotic and general stresses, which sheds light on the interpretation of their roles during hyperosmotic stress and emergency.ConclusionsSince cortisol is an important hormone for seawater acclimation as well as for general stress in teleosts, emergency and osmotic challenges could have been evolved in parallel and resulted in the overlapped signaling networks. Our results revealed important interactions among transcription factors and offer a multifactorial perspective of genes involved in seawater acclimation.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1134) contains supplementary material, which is available to authorized users.

Transcriptomic responses to environmental change in fishes: Insights from RNA sequencing

“…An extensive and rapid response of the transcriptome to high salinity was found in euryhaline medaka (Oryzias latipes; Wong et al 2014) and Asian sea bass (Lates calcarifer; Xia et al 2013). A high degree of overlap between the genes involved in signalling the osmoregulatory stress response and those related to other stressors such as handling (Wong et al 2014), bacterial infection, and fasting (Xia et al 2013), is consistent with the hypothesis that these signalling networks evolved in parallel. Metabolic pathways were widely repressed in response to stress in Asian sea bass but not in medaka, whereas immune genes were upregulated (particularly those involved in innate immunity) and downregulated in both studies.…”

“…This can make sampling protocols challenging, as any manipulations that fish experience between the environment of interest (whether in the field or laboratory) and the preservation of tissue for RNA extraction can affect gene expression. Depending on the research question, it might be prudent to collect a control sample for handling or transfer stress (e.g., Wong et al 2014) or avoid feeding prior to sampling (e.g., Liu et al 2013). …”

Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics

“…The intestine, a major osmoregulatory organ in fishes, adapts to osmolality in seawater and is involved in gene expression for salinity acclimation (Wong et al . ; Zhang et al . ), but how these processes impact the gut microbiome is still poorly understood.…”

“…Fishes live in dynamic environments where conditions such as temperature, hydrostatic pressure and salinity are highly variable . The intestine, a major osmoregulatory organ in fishes, adapts to osmolality in seawater and is involved in gene expression for salinity acclimation (Wong et al 2014;Zhang et al 2016), but how these processes impact the gut microbiome is still poorly understood. Sullam et al (2012) showed that the majority of fish gut communities clustered with free-living and non-fishassociated microbial assemblages inhabiting similar salinities as their fish host (freshwater vs marine).…”

Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish

“…OSTF1 was first identified as a salinity-induced protein in O. mossambicus gills and is orthologous to mammalian TSC22D3 (76,77,95). OSTF1 abundance also increases in other euryhaline teleosts during hyperosmotic stress (96)(97)(98)(99)(100)(101)(102). In addition to changes in mRNA abundance, phosphorylation (103) and alteration of translational preference via microRNA miR-429 (104) have been identified as mechanisms for osmotic regulation of OSTF1.…”