Transcriptome Analysis of the Nematode Caenorhabditis elegans in Acidic Stress Environments

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.

Genome-Wide Transcriptional Responses of Marine Nematode Litoditis marina to Hyposaline and Hypersaline Stresses

“…Previously, Dodd et al (2018) has shown that multiple cuticle collagen genes can be induced when C. elegans exposed to high NaCl. Recently, we reported that a battery of collagen genes in C. elegans increased their expression to deal with acidic pH stress environments ( Cong et al, 2020 ). Together, these results indicated a protective role of collagens in response to various stresses.…”

Biodiversity-based development and evolution: the emerging research systems in model and non-model organisms

“…Establishment of a terrestrial-marine relative nematodes pair model for developmental evolution and environmental adaptation C. elegans is widely used as a biomedical model organism. Its short life span, ease of handling and maintenance, clear genetic background and advanced genetic and molecular biology tools together, make C. elegans a powerful model to study development, neurobiology, longevity, and stress responses (Zhang et al, 2015b;Cong et al, 2020b). During the 20th century, the transition in biology from description to mechanistic understanding was largely due to widely employed model organisms (Russell et al, 2017).…”

“…However, the underlying mechanisms are largely unexplored. Recently, we employed RNA-Seq (RNA Sequencing) to ask how the terrestrial nematode C. elegans and the marine nematode L. marina respond to the acidic pH stresses, respectively (Cong et al, 2020b;Cong et al, 2020a). Two major response strategies to the reduced pH were found in C. elegans.…”

“…First, cuticle structure and integrity genes were significantly upregulated when the pH decreased from 6.33 to 4.33, where 6.33 is the optimal culture pH for C. elegans. Second, to deal with even lower acidic pH stress, C. elegans accelerated their xenobiotics metabolism by a large number of cytochrome P450 pathway genes (Cong et al, 2020b). C. elegans is able to grow into an adult and lay eggs at pH 3.13, while L. marina is unable to develop into adulthood at pH 4.33, appearing to be more vulnerable to acidic stress, and the number of increased P450 pathway genes in acidic pH is much lower than in C. elegans (Cong et al, 2020a;Cong et al, 2020b).…”

Genome-wide transcriptional responses of marine nematodeLitoditis marinato hyposaline and hypersaline stresses

“…Previously, Dodd et al has shown that multiple cuticle collagen genes can be induced when C. elegans exposed to high NaCl (Dodd et al, 2018). Recently, we reported that a battery of collagen genes in C. elegans increased their expression to deal with acidic pH stress environments (Cong et al, 2020). Together, these results indicated a protective role of collagens in response to various stresses.…”