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Social status affects lipid metabolism in rainbow trout, Oncorhynchus mykiss.

ABSTRACT: Juvenile rainbow trout ( Oncorhynchus mykiss) confined in pairs form social hierarchies in which socially subordinate fish display characteristic traits, including reduced growth rates and altered glucose metabolism. These effects are, in part, mediated by chronically elevated cortisol levels and/or reduced feeding. To determine the effects of social status on lipid metabolism, trout were held in pairs for 4 days, following which organismal and liver-specific indexes of lipid metabolism were measured. At the organismal level, circulating triglycerides were elevated in dominant trout, whereas subordinate trout exhibited elevated concentrations of circulating free fatty acids (FFAs) and lowered plasma total cholesterol levels. At the molecular level, increased expression of lipogenic genes in dominant trout and cpt1a in subordinate trout was identified, suggesting a contribution of increased de novo lipogenesis to circulating triglycerides in dominant trout and reliance on circulating FFAs for ?-oxidation in the liver of subordinates. Given the emerging importance of microRNAs (miRNA) in the regulation of hepatic lipid metabolism, candidate miRNAs were profiled, revealing increased expression of the lipogenic miRNA-33 in dominant fish. Because the Akt-TOR-S6-signaling pathway is an important upstream regulator of hepatic lipid metabolism, its signaling activity was quantified. However, the only difference detected among groups was a strong increase in S6 phosphorylation in subordinate trout. In general, the changes observed in lipid metabolism of subordinates were not mimicked by either cortisol treatment or fasting alone, indicating the existence of specific, emergent effects of subordinate social status itself on this fuel.

SUBMITTER: Kostyniuk DJ

PROVIDER: S-EPMC6139616 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Social status affects lipid metabolism in rainbow trout, Oncorhynchus mykiss.

Kostyniuk Daniel J DJ Culbert Brett M BM Mennigen Jan A JA Gilmour Kathleen M KM

American journal of physiology. Regulatory, integrative and comparative physiology 20180321 2

Juvenile rainbow trout ( Oncorhynchus mykiss) confined in pairs form social hierarchies in which socially subordinate fish display characteristic traits, including reduced growth rates and altered glucose metabolism. These effects are, in part, mediated by chronically elevated cortisol levels and/or reduced feeding. To determine the effects of social status on lipid metabolism, trout were held in pairs for 4 days, following which organismal and liver-specific indexes of lipid metabolism were mea ...[more]

PMID: 29561648

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Project description:Purpose: Next-generation sequencing (NGS) of small RNAs allows transcriptome level analysis of the miRNAome. The goals of this study are to identify differentially regulated hepatic miRNAs in response to a dominant or subordinate social status using small RNA next generation sequencing. Specific quantitative reverse transcription polymerase chain reaction (qRT–PCR) methods were used to validate optimal high-throughput data analysis, and in silico prediction to identify bona fide target pathways regulated by differentially regulated miRNAs following these social interactions. Method: Small RNA sequencing was performed using four randomly selected samples from each treatment group were used for sequencing. The quality of total RNA was confirmed by RNA Integrity Numbers greater than 9.0 using an Agilent Technologies 2100 Bioanalyzer. Nucleotide fractions (15-50) of small RNA were isolated from the total RNA using polyacrylamide gel electrophoresis and were ligated to a 30 adapter followed by a 50 adapter (Illumina, San Diego, CA, USA). The small RNA ligated to the adaptors was reverse transcribed to cDNA, PCR amplified and gel purified. The gel-extracted cDNA was used for library preparation, which was further used for cluster generation on Illumina's Cluster Station before sequencing using Illumina GAIIx. Raw sequence data was obtained from image data using Illumina's Sequencing Control Studio software version 2.8 (SCS v2.8) following real-time sequencing image analysis and base-calling by Illumina's Real-Time Analysis version 1.8.70 (RTA v1.8.70). The ACGT101-miR v4.2 pipeline (LC Sciences) was used to analyze sequenced data. Sequences with low Q scores, reads mapped to mRNA, RFam, Repbase and piRNA database were deleted and unique families were generated from identical sequences. These filtered unique sequences were then mapped to fish pre-miRNA and miRNA using miRBase or to the rainbow trout genome (Berthelot et al., 2014) to identify conserved miRNA following ACGT-101 User's Manual. Unique or novel miRNAs were identified after the BLAST performed against fish miRNAs from miRbase database (release 21) and published miRNAs from rainbow trout (Mennigen et al., 2016). The miRNAs that do not match any sequences in the specified databases and have the propensity of forming hairpin structure with the extended sequences at the mapped positions were classified as unique miRNAs. These unique miRNAs were further classified into different groups depending on the mappable reads to selected miRNAs in miRbase. Differentially expressed miRNAs were identified using the statistical software R (Version 3.2.2) package DESeq2 for one-way ANOVA comparison of all three treatment groups. Real-time RT–PCR validation was performed using SYBR Green assays Results: 24 miRNAs are differentially regulated by social status. 9 miRNAs are higher expressed in dominant trout. 15 miRNAs are higher expressed in subordinate trout. Conclusions: Our study represents the first detailed analysis of the rainbow trout miRNAome in response to nutritional stimuli. Specifically, we here identify common hepatic miRNAs differentially regulated by refeeding following a short-term fast (2d), as well as miRNAs differentially regulated in the postprandial state depending on the dieatary stimulus (no carbohydrates compared to >20% dietary carbohydrates)

Project description:BackgroundGenetic maps characterizing the inheritance patterns of traits and markers have been developed for a wide range of species and used to study questions in biomedicine, agriculture, ecology and evolutionary biology. The status of rainbow trout genetic maps has progressed significantly over the last decade due to interest in this species in aquaculture and sport fisheries, and as a model research organism for studies related to carcinogenesis, toxicology, comparative immunology, disease ecology, physiology and nutrition. We constructed a second generation genetic map for rainbow trout using microsatellite markers to facilitate the identification of quantitative trait loci for traits affecting aquaculture production efficiency and the extraction of comparative information from the genome sequences of model fish species.ResultsA genetic map ordering 1124 microsatellite loci spanning a sex-averaged distance of 2927.10 cM (Kosambi) and having 2.6 cM resolution was constructed by genotyping 10 parents and 150 offspring from the National Center for Cool and Cold Water Aquaculture (NCCCWA) reference family mapping panel. Microsatellite markers, representing pairs of loci resulting from an evolutionarily recent whole genome duplication event, identified 180 duplicated regions within the rainbow trout genome. Microsatellites associated with genes through expressed sequence tags or bacterial artificial chromosomes produced comparative assignments with tetraodon, zebrafish, fugu, and medaka resulting in assignments of homology for 199 loci.ConclusionThe second generation NCCCWA genetic map provides an increased microsatellite marker density and quantifies differences in recombination rate between the sexes in outbred populations. It has the potential to integrate with cytogenetic and other physical maps, identifying paralogous regions of the rainbow trout genome arising from the evolutionarily recent genome duplication event, and anchoring a comparative map with the zebrafish, medaka, tetraodon, and fugu genomes. This resource will facilitate the identification of genes affecting traits of interest through fine mapping and positional cloning of candidate genes.

Project description:BackgroundMaternal transcripts are accumulated in the oocyte during oogenesis to provide for protein synthesis from oocyte maturation through early embryonic development, when nuclear transcription is silenced. The maternal mRNAs have short poly(A) tails after undergoing post-transcriptional processing necessary for stabilizing them for storage. The transcripts undergo cytoplasmic polyadenylation when they are to be translated. Transcriptome analyses comparing total mRNA and elongated poly(A) mRNA content among eggs of different quality can provide insight into molecular mechanisms affecting egg developmental competence in rainbow trout. The present study used RNA-seq to compare transcriptomes of unfertilized eggs of rainbow trout females yielding different eyeing rates, following rRNA removal and poly(A) retention for construction of the libraries.ResultsThe percentage of embryos to reach the 32-cell stage at 24 h post fertilization was significantly correlated to family eyeing rate, indicating that inviable embryos were developmentally compromised before zygotic genome activation. RNA sequencing identified 2 differentially expressed transcripts (DETs) from total mRNA sequencing comparing females with low-quality (< 5% eyeing), medium-quality (30-50% eyeing), and high-quality (> 80% eyeing) eggs. In contrast, RNA sequencing from poly(A) captured transcripts identified 945 DETs between low- and high-quality eggs, 1012 between low- and medium-quality eggs, and only 2 between medium- and high-quality eggs. The transcripts of mitochondrial genes were enriched with polyadenylated transcript sequencing and they were significantly reduced in low-quality eggs. Similarly, mitochondrial DNA was reduced in low-quality eggs compared with medium- and high-quality eggs. The functional gene analysis classified the 945 DETs between low- and high-quality eggs into 31 functional modules, many of which were related to ribosomal and mitochondrial functions. Other modules involved transcription, translation, cell division, apoptosis, and immune responses.ConclusionsOur results indicate that differences in egg quality may be derived from differences in maternal nuclear transcript activation and cytoplasmic polyadenylation before ovulation, as opposed to accumulation and storage of maternal nuclear transcripts during oogenesis. Transcriptome comparisons suggest low-quality eggs suffered from impaired oxidative phosphorylation and translation. The DETs identified in this study provide insight into developmental competence in rainbow trout eggs.

Project description:BackgroundMicroRNAs (miRNAs) are small regulatory molecules which post-transcriptionally regulate mRNA stability and translation. Several microRNAs have received attention due to their role as key metabolic regulators. In spite of the high evolutionary conservation of several miRNAs, the role of miRNAs in lower taxa of vertebrates has not been studied with regard to metabolism. The liver-specific and highly abundant miRNA-122 is one of the most widely studied miRNA in mammals, where it has been implicated in the control of hepatic lipid metabolism. Following our identification of acute postprandial, nutritional and endocrine regulation of hepatic miRNA-122 isomiRNA expression in rainbow trout, we used complementary in silico and in vivo approaches to study the role of miRNA-122 in rainbow trout metabolism. We hypothesized that the role of miRNA-122 in regulating lipid metabolism in rainbow trout is conserved to that in mammals and that modulation of miRNA-122 function would result in altered lipid homeostasis and secondarily altered glucose homeostasis, since lipogenesis has been suggested to act as glucose sink in trout.ResultsOur results show that miRNA-122 was functionally inhibited in vivo in the liver. Postprandial glucose concentrations increased significantly in rainbow trout injected with a miRNA-122 inhibitor, and this effect correlated with decreases in hepatic FAS protein abundance, indicative of altered lipogenic potential. Additionally, miRNA-122 inhibition resulted in a 20% decrease in plasma cholesterol concentration, an effect associated with increased expression of genes involved in cholesterol degradation and excretion.ConclusionsOverall evidence suggests that miRNA-122 may have evolved in early vertebrates to support liver-specific metabolic functions. Nevertheless, our data also indicate that metabolic consequences of miRNA-122 inhibition may differ quantitatively between vertebrate species and that distinct direct molecular targets of miRNA-122 may mediate metabolic effects between vertebrate species, indicating that miRNA-122 - mRNA target relationships may have undergone species-specific evolutionary changes.

Dataset Information

Social status affects lipid metabolism in rainbow trout, Oncorhynchus mykiss.

Publications

Social status affects lipid metabolism in rainbow trout, Oncorhynchus mykiss.

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