Transcriptome Analysis of the Nematode Caenorhabditis elegans in Acidic Stress Environments.

Yanyi Cong,Yusu Xie,Liusuo Zhang,Pengchi Zhang,Xuwen Cao,Hanwen Yang

doi:10.3389/fphys.2020.01107

Abstract

Ocean acidification and acid rain, caused by modern industries’ fossil fuel burning, lead to a decrease in the living environmental pH, which results in a series of negative effects on many organisms. However, the underlying mechanisms of animals’ response to acidic pH stress are largely unknown. In this study, we used the nematode Caenorhabditis elegans as an animal model to explore the regulatory mechanisms of organisms’ response to pH decline. Two major stress-responsive pathways were found through transcriptome analysis in acidic stress environments. First, when the pH dropped from 6.33 to 4.33, the worms responded to the pH stress by upregulation of the col, nas, and dpy genes, which are required for cuticle synthesis and structure integrity. Second, when the pH continued to decrease from 4.33, the metabolism of xenobiotics by cytochrome P450 pathway genes (cyp, gst, ugt, and ABC transporters) played a major role in protecting the nematodes from the toxic substances probably produced by the more acidic environment. At the same time, the slowing down of cuticle synthesis might be due to its insufficient protective ability. Moreover, the systematic regulation pattern we found in nematodes might also be applied to other invertebrate and vertebrate animals to survive in the changing pH environments. Thus, our data might lay the foundation to identify the master gene(s) responding and adapting to acidic pH stress in further studies, and might also provide new solutions to improve assessment and monitoring of ecological restoration outcomes, or generate novel genotypes via genome editing for restoring in challenging environments especially in the context of acidic stress through global climate change.

Highlights

As an essential environmental factor, pH affects many life processes such as growth, development, metabolism, as well as immune regulation
We found that there might be two major strategies C. elegans used to deal with pH stress: first, the expression level of cuticle structure and integrity-related genes was significantly increased when pH declined from 6.33 to 4.33; second, to deal with even lower pH stress, C. elegans substantially increased their xenobiotic metabolism by cytochrome P450 pathway genes
Our results showed that C. elegans is highly resistant to pH stress, and it can grow and reproduce in a wide range of pH (3.13–11.33) (Figure 1)

Summary

Introduction

As an essential environmental factor, pH affects many life processes such as growth, development, metabolism, as well as immune regulation. Whether on land or in water, living organisms often experience pH fluctuations. In recent years, increasing carbon dioxide emissions contribute to ocean acidification and increase the challenges of living environment pressures faced by marine. Due to the increase in H+, the marine chemical balance will be broken down, making a variety of marine organisms and even ecosystems that depend on the stability of the chemical environment face great threats (Cornwall and Eddy, 2015; Doubleday et al, 2018). A decrease in the pH of seawater can seriously affect the survival and development of larvae of Atlantic cod, causing damage to important organs such as gills and liver (Stiasny et al, 2018). The decrease in pH has a negative impact on the metamorphosis of Pacific oyster larvae by downregulating several proteins involved in energy production, metabolism, and protein synthesis (Dineshram et al, 2016)

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Results

Conclusion