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Comparative Study
. 2022 Jan 7;12(1):121.
doi: 10.1038/s41598-021-03306-8.

Tenebrio molitor larvae meal inclusion affects hepatic proteome and apoptosis and/or autophagy of three farmed fish species

Eleni Mente  1   2 , Thomas Bousdras  3 , Konstantinos Feidantsis  3 , Nikolas Panteli  3 , Maria Mastoraki  3 , Konstantinos Ar Kormas  4 , Stavros Chatzifotis  5 , Giovanni Piccolo  6 , Laura Gasco  7 , Francesco Gai  8 , Samuel A M Martin  9 , Efthimia Antonopoulou  3
Affiliations
Comparative Study

Tenebrio molitor larvae meal inclusion affects hepatic proteome and apoptosis and/or autophagy of three farmed fish species

Eleni Mente et al. Sci Rep. .

Abstract

Herein, the effect of dietary inclusion of insect (Tenebrio molitor) meal on hepatic pathways of apoptosis and autophagy in three farmed fish species, gilthead seabream (Sparus aurata), European seabass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss), fed diets at 25%, 50% and 60% insect meal inclusion levels respectively, was investigated. Hepatic proteome was examined by liver protein profiles from the three fish species, obtained by two-dimensional gel electrophoresis. Although cellular stress was evident in the three teleost species following insect meal, inclusion by T. molitor, D. labrax and O. mykiss suppressed apoptosis through induction of hepatic autophagy, while in S. aurata both cellular procedures were activated. Protein abundance showed that a total of 30, 81 and 74 spots were altered significantly in seabream, European seabass and rainbow trout, respectively. Insect meal inclusion resulted in individual protein abundance changes, with less number of proteins altered in gilthead seabream compared to European seabass and rainbow trout. This is the first study demonstrating that insect meal in fish diets is causing changes in liver protein abundances. However, a species-specific response both in the above mentioned bioindicators, indicates the need to strategically manage fish meal replacement in fish diets per species.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
A representative two-dimensional gel of liver proteins of (a) gilthead seabream (Sparus aurata), (b) European seabass (Dicentrarchus labrax) and (c) rainbow trout (Oncorhynchus mykiss) fed 0% inclusion of T. molitor (TM) meal. Protein spots showing significant changes in their abundance are indicated by a number.
Figure 2
Figure 2
PCA changes in abundance of proteins spots. The 2D gel images were grouped per dietary inclusion of T. molitor (TM) meal for (a) gilthead seabream (Sparus aurata), (b) European seabass (Dicentrarchus labrax) and (c) rainbow trout (Oncorhynchus mykiss). The locations of the significantly different protein spots (expressed as mean normalised values) [Progenesis SameSpots version 4.5 (Non-linear Dynamics, Newcastle upon Tyne, UK www.nonlinear.com)] from four or five gel images per dietary treatment were used.
Figure 3
Figure 3
(a) Bax, (b) Bcl-2, (c) Bax/Bcl-2 ratio and (d) caspases in the liver of gilthead seabream (Sparus aurata), European seabass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss) under the 0–25%, 0–50% and 0–60% respectively inclusion of T. molitor (TM) meal. Representative immunoblots (Western blot for Bax and Bcl-2; Dot blot for caspases) are shown and were quantified by laser scanning [Gel-Pro Analyzer 4.0 software (Media Cybernetics, Inc. www.mediacy.com)] and plotted [SigmaPlot 12.5 software (Systat Software Inc. www.systatsoftware.com)]. Values represent means ± SD; n = 5 preparations from different animals. Data was statistically analyzed [GraphPad Instat 3.10 (GraphPad Software, www.graphpad.com)]: *denotes significant differences (p < 0.05) compared with 0%. The accompanying tables exhibit fold-differences between TM diet inclusion and control (0%). s, d and o denote significant differences (p < 0.05) between S. aurata, D. labrax and O. mykiss, respectively.
Figure 4
Figure 4
(a) Ubiquitin conjugates, (b) LC3BII/LC3BI ratio and (c) SQSTM1/p62 in the liver of gilthead seabream (Sparus aurata), European seabass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss) under the 0–25%, 0–50% and 0–60% respectively inclusion of T. molitor (TM) meal. Representative immunoblots (Western blot for LC3BII/LC3BI and SQSTM1/p62; Dot blot for ubiquitin cojuagates) are shown and were quantified by laser scanning densitometry [Gel-Pro Analyzer 4.0 software (Media Cybernetics, Inc. www.mediacy.com)] and plotted [SigmaPlot 12.5 software (Systat Software Inc. www.systatsoftware.com)]. Values represent means ± SD; n = 5 preparations from different animals. Data was statistically analyzed [GraphPad Instat 3.10 (GraphPad Software, www.graphpad.com)]: *denotes significant differences (p < 0.05) compared with 0%. The accompanying tables exhibit fold-differences between TM diet inclusion and control (0%). s, d and o denote significant differences (p < 0.05) between S. aurata, D. labrax and O. mykiss, respectively.
Figure 5
Figure 5
Graphical representation of the effect of Tenebrio molitor (TM) dietary inclusion on the hepatic apoptosis and autophagy, and the hepatic proteome profile of gilthead seabream (Sparus aurata), European seabass (Dicentrarchus labrax) the rainbow trout (Oncorhynchus mykiss). Photographs of T. molitor (TM) meal, fish species investigated, and liver form each species are copyright of our laboratory.
See this image and copyright information in PMC

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