Understanding pseudo-albinism in sole (Solea senegalensis): a transcriptomics and metagenomics approach

Patricia I S Pinto,Cláudia C Guerreiro,Carlos Carballo,Deborah M Power,Rita A Costa,Juan F Martinez-Blanch,Manuel Manchado,Francisco M Codoñer

doi:10.1038/s41598-019-49501-6

Abstract

Pseudo-albinism is a pigmentation disorder observed in flatfish aquaculture with a complex, multi-factor aetiology. We tested the hypothesis that pigmentation abnormalities are an overt signal of more generalised modifications in tissue structure and function, using as a model the Senegalese sole and two important innate immune barriers, the skin and intestine, and their microbiomes. Stereological analyses in pseudo-albino sole revealed a significantly increased mucous cell number in skin (P < 0.001) and a significantly thicker muscle layer and lamina propria in gut (P < 0.001). RNA-seq transcriptome analysis of the skin and gut identified 573 differentially expressed transcripts (DETs, FDR < 0.05) between pseudo-albino and pigmented soles (one pool/tissue from 4 individuals/phenotype). DETs were mainly linked to pigment production, skin structure and regeneration and smooth muscle contraction. The microbiome (16 S rRNA analysis) was highly diverse in pigmented and pseudo-albino skin but in gut had low complexity and diverged between the two pigmentation phenotypes. Quantitative PCR revealed significantly lower loads of Mycoplasma (P < 0.05) and Vibrio bacteria (P < 0.01) in pseudo-albino compared to the control. The study revealed that pseudo-albinism in addition to pigmentation changes was associated with generalised changes in the skin and gut structure and a modification in the gut microbiome.

Highlights

Flatfish are a fascinating model in which to investigate factors that govern body symmetry and pigmentation patterns in vertebrates
This action is antagonized by the paracrine factor agouti-signalling protein (ASIP1) that competes with α-melanophore-stimulating hormone (MSH) for melanocortin 1 receptor (MC1R) binding
To assess the long-lasting morphological, microbial and expression patterns that occur in pseudo-albino juvenile soles, specimens cultivated under the same conditions for six months were randomly chosen from the rearing tank

Summary

Introduction

Flatfish are a fascinating model in which to investigate factors that govern body symmetry and pigmentation patterns in vertebrates. The lack of melanin production in skin is the most evident effect in pseudo-albinism, the disruption of the melanocortin regulatory pathway can affect feeding behaviour, growth, stress and the immune response[15,16]. This leads us to hypothesize that pseudo-albinism in fish is the visual manifestation of changes in skin and other tissues and, in the case of those in contact with the environment, may modify their microbial community. To assess if modified pigmentation in pseudo-albino fish was associated with changes in the microbiome, 16 S rRNA gene amplification coupled to high-throughput sequencing and quantitative PCR validation was performed for the skin and gut in this flatfish species

Methods

Results

Discussion

Conclusion