Gill transcriptomic analysis in fast- and slow-growing individuals of Mytilus galloprovincialis

Abstract

The molecular basis underlying the mechanisms at the origin of growth variation in bivalves is still poorly understood, although several genes have been described as upregulated in fast-growing individuals. 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 from each condition were selected to obtain 4 experimental groups: FBP, SBP, FAP and SAP. We hypothesized that the nurturing conditions during the growing period would modify the molecular basis of their growth rate differences. To decipher the molecular mechanisms underlying the growth variation, the gill transcriptomes for the four mussel groups were analysed. Gene expression analysis revealed i) a low number (12) of genes differentially expressed in association with diet and ii) 117 genes differentially expressed by the fast-and slow-growing mussels. According to Biological Process GO term analysis transcriptomic differences between the F and S mussels were mainly based on the upregulation of: response to the stimulus, growth and cell activity. Regarding the KEGG terms, carbohydrate metabolism and the Krebs cycle were upregulated in F mussels, whereas biosynthetic processes were upregulated in S mussels. In accordance with their larger gill surface area and higher rates of feeding and growth, the F individuals overexpressed genes in their gill tissues, and these were involved in i) growth (insulin-like growth factors and myostatin); ii) maintenance of the structure and functioning of extracellular matrix (collagen, laminin, fibulin and decorin); iii) filtration and ciliary activity (mucin, fibrocystin, dynein and tilB homolog protein genes); iv) aerobic metabolism (citrate synthase and carbonic anhydrase); and v) the immune-system, probably in association with haemocytes. In contrast, S individuals overexpressed a different series of genes pertaining to immune system (leucine-rich repeat protein and galectin), along with genes involved in the response to cellular stress (Heat shock protein (HSP24) and metalloendopeptidase) as well as anaerobic metabolism (C4-dicarboxylate transporter). These results might suggest that S individuals would have a greater prevalence of pathogens/diseases or a higher susceptibility to the pathogens. Highlights ► Fast-and slow-growing mussel (Mytilus galloprovincialis) spat were found to differentially express 117 genes in gill tissue. ► Fast-growing mussels overexpressed genes involved in response to stimulus,growth and cell activity processes. ► Slow-growing mussels overexpressed genes involved in immune and defence processes. ► Feeding above or below the pseudofaeces production threshold did not exert a relevant effect on the gill transcriptome.

Nature more than nurture affects the growth rate of mussels

“…The difference in the immune responses found between fast and slow growing specimens revealed by a gill-transcriptomic analysis in Prieto et al 17 constitutes a relevant endogenous factor causing inter-individual differences in the growth potential of the mussels from the present experiments and might also explain those observed in Prieto et al 8 . A putative, higher metabolic requirement linked to a less-efficient immune system could be a relevant physiological factor limiting the scope for growth of S individuals and could ultimately promote the size-differentiation between F and S specimens.…”

“…This result is entirely consistent with the physiological data showing that fast growth is based, irrespective of the maintenance condition, on the capacity of F specimens to display higher clearance rates and selection efficiencies than S specimens. An analysis of the transcriptome of the gills of these experimental mussels 17 has shown the existence of broad differences in the genetic expression of the gill tissue between fast and slow growing specimens that likely explain the corresponding physiological and morphometric differences: the gills of S mussels suffer a greater stress either because they have a greater prevalence of pathogens/diseases or because they have a higher susceptibility to pathogens that force them to devote more metabolic energy to the maintenance of immune and defence processes to ensure survival at the expense of growth rate.…”

“…The power function that scales gill area to live weight is 0.66 [42][43][44] . Gills were dissected, then immersed in RNA and used for gill-transcriptomic analysis 17 .…”

“…Growth is a complex phenotypic trait likely controlled by several genetic factors. Not surprisingly, gene expression rates obtained from transcriptomic analysis have shown that fast (F) and slow (S) growing specimens differ in the expression of large amounts (up to thousands) of genes involved in many biological functions [14][15][16][17] .…”

“…To further analyse how physiologic, genetic and environment interactions determine fast growing in the mussel M.galloprovincialis, Prieto et al ( 8,17 and present study) designed a series of long-lasting laboratory experiments where stocks of juvenile specimens were reared and left to size-differentiate (F vs S) under a set of different experimental conditions. In Prieto et al 8 , we reported the results obtained with two groups of mussels that were reared in the laboratory under moderate and severe food-restrictive conditions.…”