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Chronic exposure to high-density polyethylene microplastic through feeding alters the nutrient metabolism of juvenile yellow perch (Perca flavescens) - PubMed

  • ️Sat Jan 01 2022

doi: 10.1016/j.aninu.2022.01.007. eCollection 2022 Jun.

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Chronic exposure to high-density polyethylene microplastic through feeding alters the nutrient metabolism of juvenile yellow perch (Perca flavescens)

Xing Lu et al. Anim Nutr. 2022.

Abstract

Microplastics are emergent contaminants threatening aquatic organisms including aquacultured fish. This study investigated the effects of high-density polyethylene (HDPE, 100 to 125 μm) on yellow perch (Perca flavescens) based on integrative evaluation including growth performance, nutritional status, nutrient metabolism, fish health, and gut microbial community. Five test diets (0, 1, 2, 4, or 8 g HDPE/100 g diet) containing 41% protein and 10.5% lipid were fed to juvenile perch (average body weight, 25.9 ± 0.2 g; n = 15) at a feeding rate of 1.5% to 2.0% body weight daily. The feeding trial was conducted in a flow-through water system for 9 wk with 3 tanks per treatment and 15 yellow perch per tank. No mortality or HDPE accumulation in the fish was found in any treatments. Weight gain and condition factor of fish were not significantly impacted by HDPE (P > 0.05). Compared to the control group, fish fed the 8% HDPE diet had significantly decreased levels of protein and ash (P < 0.05). In response to the increasing levels of HDPE exposure, the hepatosomatic index value, hepatocyte size, and liver glycogen level were increased, but lipid content was reduced in the liver tissues. Compared to the control treatment, fish fed the 8% HDPE diet had significant accumulations of total bile acids and different metabolism pathways such as bile acid biosynthesis, pyruvate metabolism, and carnitine synthesis. Significant enterocyte necrosis was documented in the foregut of fish fed the 2% or 8% HDPE diet; and significant cell sloughing was observed in the midgut and hindgut of fish fed the 8% HDPE diet. Fish fed the 2% HDPE diet harbored different microbiota communities compared to the control fish. This study demonstrates that HDPE ranging from 100 to 125 μm in feed can be evacuated by yellow perch with no impact on growth. However, dietary exposure to HDPE decreased whole fish nutrition quality, altered nutrient metabolism and the intestinal histopathology as well as microbiota community of yellow perch. The results indicate that extended exposure may pose a risk to fish health and jeopardize the nutrition quality of aquacultured end product. This hypothesis remains to be investigated further.

Keywords: Dietary exposure; Intestinal microbiota; Liver metabolomics; Microplastics; Nutrient composition; Yellow perch.

© 2022 Chinese Association of Animal Science and Veterinary Medicine. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co. Ltd.

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Conflict of interest statement

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the content of this paper.

Figures

Image 1
Graphical abstract
Fig. 1
Fig. 1

Image of standard high-density polyethylene detected (HDPE), cellulose, and HDPE extracted from test diets. (A) commercial pure HDPE added to the test diets; (B) cellulose; (C) 0% HDPE diet with no added HDPE; (D) 1% HDPE; (E) 2% HDPE; (F) 4% HDPE; (G) 8% HDPE. Magnification = 32× for all pictures.

Fig. 2
Fig. 2

Livers of yellow perch fed various test diets for 9 wk. Hepatocyte diameter and number of Kupffer cells were identified in a 10,000 mm2 area of similar location on each serial section. (A) Diet 1, no added HDPE; (B) Diet 2, 1% HDPE; (C) Diet 3, 2% HDPE; (D) Diet 4, 4% HDPE; (E) Diet 5, 8% HDPE. (F) A higher magnification picture of Diet 2. G = glycogen; KC = Kupffer cell; LV = Lipid vacuoles.

Fig. 3
Fig. 3

(A) A whole intestine of yellow perch and (B) a cross-section of intestine for morphology measurements. Three selected portions of intestine sample (about 1 cm length) collection representing foregut, midgut, and hindgut for histology assay.

Fig. 4
Fig. 4

(A) 1D 1H Nuclear Magnetic Resonance (NMR) spectra recorded using a 700 MHz NMR spectrometer on polar liver extracts of yellow perch fed diet 1 (D1), diet 3 (D3), and diet 5 (D5) for 9 wk. Identified metabolites are annotated. (B) Summary plot for Quantitative Enrichment Analysis (QEA) based on a list of 20 metabolites detected by NMR in yellow perch liver extracts. BA = bile acids; HDPE = high-density polyethylene.

Fig. 5
Fig. 5

(A) Principal Component Analysis and (B) Partial Least Square Discriminant Analysis (PLS-DA) score plots derived from Nuclear Magnetic Resonance (NMR) spectra of liver extracts from yellow perch fed D1 (0% HDPE), D3 (2% HDPE) or D5 (8% HDPE) for 9 wk. Circles represent individual liver samples and NMR spectra. Shaded areas represent the 95% confidence regions for each group. Permutation testing (n = 100, P = 0.02) was performed for PLS-DA model validation. (C). Relative levels of total bile acids in liver extracts of yellow perch fed D1, D3, or D5 for 9 wk. P-values were calculated using a t-test (letters of a and b indicted statistical significance at P < 0.05 among treatment). HDPE = high-density polyethylene.

Fig. 6
Fig. 6

Gastrointestinal tracts of yellow perch fed control diet showing (A) foregut, (B) midgut, and (C) hindgut of yellow perch. Scale bar = 200 μm. (D) Higher magnification of foregut showing the mucosa layer of foregut with highly branched, elongated, and finger like villi (arrows) and few goblet cells scattered among the enterocytes. Scale bar = 40 μm. (E) Higher magnification of midgut showing flatter villi with large number of goblet cells in the midgut. Scale bar = 40 μm. (F) Higher magnification of hindgut showing reduction in goblet cells and increase in vacuolated enterocytes (VC) in the hindgut. Scale bar = 40 μm. FD = food in the lumen.

Fig. 7
Fig. 7

Gastrointestinal tracts of Yellow Perch fed 8% HDPE diet showing (A) moderate to severe necrosis of enterocytes (ECN) in the foregut (scale bar = 50 μm) and (B) severe infiltration of inflammatory cells (arrows) and cell sloughing (CS) in the hindgut (scale bar = 100 μm).

Fig. 8
Fig. 8

(A) Stacked bar plot of bacterial relative abundance at the family-level of taxonomic assignment, and (B) a heatmap of the top 5 most abundant amplicon sequence variants (ASV) in each sample across all samples. ASV clustering by relative abundance pattern is displayed with a dendrogram and the most refined taxonomic classification is listed. Yellow perch fed diets containing 0%, 2%, or 8% of HDPE 9 wk. HDPE = high-density polyethylene.

Fig. 9
Fig. 9

(A) Box plot of the bacterial community alpha diversity (Shannon index). All measurements are indicated as points, and the box plot indicates median, and the 1st and 3rd quartiles within each diet group Significant differences (P ≤ 0.05) among diet groups is indicated with an asterisk and ns = not significantly different (Wilcoxon rank sum test). (B) Non-metric multidimensional scaling plot, NMDS of bacterial community beta diversity among diet treatments. Ellipses contain all samples in a given diet condition. Yellow perch fed diets containing 0%, 2%, or 8% of HDPE 9 wk. HDPE = high-density polyethylene.

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