Dose-effect of polystyrene microplastics on digestive toxicity in chickens (Gallus gallus): Multi-omics reveals critical role of gut-liver axis <sup>☆</sup>

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Graphical abstract

Highlights

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Molecular toxicity of microplastic to the avian digestive system was characterized.
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Unlike other species, microplastic caused intestinal necrosis and pyroptosis in avian.
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The avian liver toxicity caused by microplastic is lipid metabolism disorder and apoptosis.
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The gut microbiota participates in microplastic induced liver injury by the gut-liver axis.
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Caffeine and melanin may be potential natural resistances to microplastic toxicity.

Abstract

Introduction

Microplastic pollution seriously threatens the health and safety of humans and wildlife. Avian is one of the main species endangered by microplastics. However, the damage mechanism of microplastics to the digestive system of avian is not clear.

Objectives

The gut-liver axis is a bidirectional channel that regulates the exchange of information between the gut and the liver and is also a key target for tissue damage caused by pollutants. This study aimed to elucidate the digestive toxicity of microplastics in avian and the key role of the gut-liver axis in it.

Methods

We constructed an exposure model for microplastics in environmental concentrations and toxicological concentrations in chickens and reveal the digestive toxicity of polystyrene microplastics (PS-MPs) in avian by 16S rRNA, transcriptomics and metabolomics.

Results

PS-MPs changed the death mode from apoptosis to necrosis and pyroptosis by upregulating Caspase 8, disrupting the intestinal vascular barrier, disturbing the intestinal flora and promoting the accumulation of lipopolysaccharide. Harmful flora and metabolites were translocated to the liver through the liver-gut axis, eliciting hepatic immune responses and promoting hepatic lipid metabolism disorders and apoptosis. Liver injury involves multiple molecular effects of mitochondrial dynamics disturbance, oxidative stress, endoplasmic reticulum stress, and cell cycle disturbance. Furthermore, metabolomics suggested that caffeine and melanin metabolites may be potential natural resistance substances for microplastics.

Conclusion

Taken together, our data demonstrate the digestive damage of PS-MPs in avian, revealing a critical role of the liver-gut axis in it. This will provide a reference for protecting the safety of avian populations.

Related collections

Most cited references 79

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Microplastics in freshwater and terrestrial environments: Evaluating the current understanding to identify the knowledge gaps and future research priorities.

Alice A Horton, Alexander Walton, David J Spurgeon … (2017)

Plastic debris is an environmentally persistent and complex contaminant of increasing concern. Understanding the sources, abundance and composition of microplastics present in the environment is a huge challenge due to the fact that hundreds of millions of tonnes of plastic material is manufactured for societal use annually, some of which is released to the environment. The majority of microplastics research to date has focussed on the marine environment. Although freshwater and terrestrial environments are recognised as origins and transport pathways of plastics to the oceans, there is still a comparative lack of knowledge about these environmental compartments. It is highly likely that microplastics will accumulate within continental environments, especially in areas of high anthropogenic influence such as agricultural or urban areas. This review critically evaluates the current literature on the presence, behaviour and fate of microplastics in freshwater and terrestrial environments and, where appropriate, also draws on relevant studies from other fields including nanotechnology, agriculture and waste management. Furthermore, we evaluate the relevant biological and chemical information from the substantial body of marine microplastic literature, determining the applicability and comparability of this data to freshwater and terrestrial systems. With the evidence presented, the authors have set out the current state of the knowledge, and identified the key gaps. These include the volume and composition of microplastics entering the environment, behaviour and fate of microplastics under a variety of environmental conditions and how characteristics of microplastics influence their toxicity. Given the technical challenges surrounding microplastics research, it is especially important that future studies develop standardised techniques to allow for comparability of data. The identification of these research needs will help inform the design of future studies, to determine both the extent and potential ecological impacts of microplastic pollution in freshwater and terrestrial environments.

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Cyriac Kandoth, Michael D. McLellan, Fabio Vandin … (2013)

The Cancer Genome Atlas (TCGA) has used the latest sequencing and analysis methods to identify somatic variants across thousands of tumours. Here we present data and analytical results for point mutations and small insertions/deletions from 3,281 tumours across 12 tumour types as part of the TCGA Pan-Cancer effort. We illustrate the distributions of mutation frequencies, types and contexts across tumour types, and establish their links to tissues of origin, environmental/carcinogen influences, and DNA repair defects. Using the integrated data sets, we identified 127 significantly mutated genes from well-known(forexample, mitogen-activatedprotein kinase, phosphatidylinositol-3-OH kinase,Wnt/β-catenin and receptor tyrosine kinase signalling pathways, and cell cycle control) and emerging (for example, histone, histone modification, splicing, metabolism and proteolysis) cellular processes in cancer. The average number of mutations in these significantly mutated genes varies across tumour types; most tumours have two to six, indicating that the numberof driver mutations required during oncogenesis is relatively small. Mutations in transcriptional factors/regulators show tissue specificity, whereas histone modifiers are often mutated across several cancer types. Clinical association analysis identifies genes having a significant effect on survival, and investigations of mutations with respect to clonal/subclonal architecture delineate their temporal orders during tumorigenesis. Taken together, these results lay the groundwork for developing new diagnostics and individualizing cancer treatment.

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The gut-liver axis in liver disease: pathophysiological basis for therapy

Agustin Albillos, Andrea De Gottardi, Maria Rescigno (2019)

The gut-liver axis refers to the bidirectional relationship between the gut and its microbiota, and the liver, resulting from the integration of signals generated by dietary, genetic and environmental factors. This reciprocal interaction is established by the portal vein which enables transport of gut-derived products directly to the liver, and the liver feedback route of bile and antibody secretion to the intestine. The intestinal mucosal and vascular barrier is the functional and anatomical structure that serves as a playground for the interactions between the gut and the liver, limiting the systemic dissemination of microbes and toxins while allowing nutrients to access the circulation and to reach the liver. The control of microbial communities is critical to maintaining homeostasis of the gut-liver axis, and as part of this bidirectional communication the liver shapes intestinal microbial communities. Alcohol disrupts the gut-liver axis at multiple interconnected levels, including the gut microbiome, mucus barrier, epithelial barrier and at the level of antimicrobial peptide production, which increases microbial exposure and the proinflammatory environment of the liver. Growing evidence indicates the pathogenetic role of microbe-derived metabolites, such as trimethylamine, secondary bile acids, short-chain fatty acids and ethanol, in the pathogenesis of non-alcoholic fatty liver disease. Cirrhosis by itself is associated with profound alterations in gut microbiota and damage at the different levels of defence of the intestinal barrier, including the epithelial, vascular and immune barriers. The relevance of the severe disturbance of the intestinal barrier in cirrhosis has been linked to translocation of live bacteria, bacterial infections and disease progression. The identification of the elements of the gut-liver axis primarily damaged in each chronic liver disease offers possibilities for intervention. Beyond antibiotics, upcoming therapies centred on the gut include new generations of probiotics, bacterial metabolites (postbiotics), faecal microbial transplantation, and carbon nanoparticles. FXR-agonists target both the gut and the liver and are currently being tested in different liver diseases. Finally, synthetic biotic medicines, phages that target specific bacteria or therapies that create physical barriers between the gut and the liver offer new therapeutic approaches.

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Author and article information

Contributors

Yu Wang

Mingwei Xing

Journal

Journal ID (nlm-ta): J Adv Res

Journal ID (iso-abbrev): J Adv Res

Title: Journal of Advanced Research

Publisher: Elsevier

ISSN (Print): 2090-1232

ISSN (Electronic): 2090-1224

Publication date PMC-release: 09 November 2022

Publication date Collection: October 2023

Publication date (Electronic): 09 November 2022

Volume: 52

Pages: 3-18

Affiliations

College of Wildlife and Protected Area, Northeast Forestry University, Harbin 150040, Heilongjiang, PR China

Author notes

[* ]Corresponding authors at: College of Wildlife and Protected Area, Northeast Forestry University, Harbin 150040, Heilongjiang, PR China. wangyu2013@ 123456nefu.edu.cn xingmingwei@ 123456nefu.edu.cn

Article

Publisher Item ID: S2090-1232(22)00244-2

DOI: 10.1016/j.jare.2022.10.015

PMC ID: 10555772

PubMed ID: 36334886

SO-VID: e16cb0fb-996b-48ca-bc91-d4773df7fe98

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 26 July 2022

Date revision received : 19 September 2022

Date accepted : 28 October 2022

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