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Effects of Changes in Food Supply at the Time of Sex Differentiation on the Gonadal Transcriptome of Juvenile Fish. Implications for Natural and Farmed Populations

ABSTRACT: Background: Food supply is a major factor influencing growth rates in animals. This has important implications for both natural and farmed fish populations, since food restriction may difficult reproduction. However, a study on the effects of food supply on the development of juvenile gonads has never been transcriptionally described in fish. Methods and Findings: This study investigated the consequences of growth on gonadal transcriptome of European sea bass in: 1) 4-month-old sexually undifferentiated fish, comparing the gonads of fish with the highest vs. the lowest growth, to explore a possible link between transcriptome and future sex, and 2) testis from 11-month-old juveniles where growth had been manipulated through changes in food supply. The four groups used were: i) sustained fast growth, ii) sustained slow growth, iii) accelerated growth, iv) decelerated growth. The transcriptome of undifferentiated gonads was not drastically affected by initial natural differences in growth. Further, changes in the expression of genes associated with protein turnover were seen, favoring catabolism in slow-growing fish and anabolism in fast-growing fish. Moreover, while fast-growing fish took energy from glucose, as deduced from the pathways affected and the analysis of protein-protein interactions examined, in slow-growing fish lipid metabolism and gluconeogenesis was favored. Interestingly, the highest transcriptomic differences were found when forcing initially fast-growing fish to decelerate their growth, while accelerating growth of initially slow-growing fish resulted in full transcriptomic convergence with sustained fast-growing fish. Conclusions: Food availability during sex differentiation shapes the juvenile testis transcriptome, as evidenced by adaptations to different energy balances. Remarkably, this occurs in absence of major histological changes in the testis. Thus, fish are able to recover transcriptionally their testes if they are provided with enough food supply during sex differentiation; however, an initial fast growth does not represent any advantage in terms of transcriptional fitness if later food becomes scarce.

ORGANISM(S): Dicentrarchus labrax

PROVIDER: GSE54362 | GEO | 2014/12/25

SECONDARY ACCESSION(S): PRJNA236318

REPOSITORIES: GEO

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Project description:Endogenously determined inter-individual differences in growth rate of bivalve molluscs have been widely analyzed at different organizational levels. Most studies have focused on the characterization of the physiological differences between fast (F) and slow (S) growing individuals. Although several genes have been described to be up regulated on fast growing individuals, the molecular basis underlying the mechanisms at the origin of growth variation is still poorly understood. In the present study we reared mussel spat of the species Mytilus galloprovincialis under diets below the pseudofaeces threshold (BP) and above the pseudofaeces threshold (AP). After 3 months, F and S mussels on each condition were selected, so that 4 experimental groups were obtained: FBP, SBP, FAP and SAP. We hypothesized that nurturing conditions during their growing period would modify the molecular basis of growth rate differences. However, results of feeding experiments showed that F mussels displayed higher clearance and ingestion rates and higher efficiencies of food selection prior to ingestion, as well as higher gill surface areas, irrespective of the rearing nutritional environment. To decipher molecular mechanism at the origin of growth variation, gills of the 4 mussel groups were dissected, and used for transcriptome analysis with a custom Agilent single channel microarray. Gene expression analysis revealed i) a low number (12) of genes differentially expressed associated to maintenance condition differences and ii) 117 genes differentially expressed when comparing fast and slow growing mussels (FBP + FAP vs. SBP + SAP). We further investigated this comparison: GO terms and KEGG pathway association of the differentially expressed genes allowed us to analyze the functions involved on the differentially expressed encoding. Transcriptomic differences between F and S mussels were mainly based on the up-regulation of response to stimulus, growth and cell activity Biological Process GO terms. Regarding the KEGG terms, carbohydrate metabolism and Krebs cycle were found to be up-regulated in F mussels whereas biosynthetic processes were up-regulated in S mussels. Among the differentially expressed genes that are annotated, the following ones were found to be up regulated in F mussels: i) Mucin, related to mucus secretion, known to be crucial in food acquisition and pre-ingestive selection processes in bivalves, ii) genes related to growth such as Myostatin or Insulin-like growth factor, iii) genes involved in feeding activity, such as Fibrocystin or Dynein and iv) genes involved in the energetic metabolism; Citrate synthase. S mussels mainly over-expressed genes related to immune system and defence (Leucine-rich repeat-containing protein, Metalloendopeptidase, Small heat shock protein 24, Multidrug resistance,…).The present results suggest that differences in feeding activity and in the allocation of metabolic energy between growth groups could account for the differences in growth rate in spat of Mytilus galloprovincialis. In accordance with their higher feeding rates and growth, fast growing mussels were found to mainly over-express genes involved in the development and maintenance of such activities, however, slow growing mussels needed to expend energy in immune and defence processes to ensure survival at the expense of growth rate.

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Effects of Changes in Food Supply at the Time of Sex Differentiation on the Gonadal Transcriptome of Juvenile Fish. Implications for Natural and Farmed Populations

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