Dataset Information

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.

SUBMITTER: Cong Y

PROVIDER: S-EPMC7511720 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Transcriptome Analysis of the Nematode <i>Caenorhabditis elegans</i> in Acidic Stress Environments.

Cong Yanyi Y Yang Hanwen H Zhang Pengchi P Xie Yusu Y Cao Xuwen X Zhang Liusuo L

Frontiers in physiology 20200910

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 <i>Caenorhabditis elegans</i> as an animal model to explore the regulatory mechanisms of organisms' response to pH decline. Two major stress-responsive pathways were ...[more]

PMID: 33013473

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Project description:In the past decade, the paradigm which claimed that invertebrate immune systems lack specificity has been reconsidered. Accumulating evidence supports that invertebrate immune systems are able to mount specific responses to the pathogen species-, and even to the pathogen strain-level. However, the underlying molecular mechanisms behind invertebrate immune specificity remain mostly unknown. Studying the molecular basis of invertebrate immune specificity in a genetically tractable model, such as the nematode Caenorhabditis elegans, has the potential to reveal insights into the immune systems of other metazoans, including humans. We chose to study the mechanisms of specific immune responses of the worm to two different pathogenic strains of the Gram-positive bacterium Bacillus thuringiensis (MYBY18247 and MYBT18679), because there is phenotypic evidence of specific genotype-genotype interactions between this host-pathogen pair. We did an initial RNA-Seq experiment upon pathogen exposure and found that 9% of the differentially expressed genes change their expression in different ways when comparing the two pathogen strains. Through promoter region motif enrichment analysis, we found the GATA transcription factor ELT-2 is responsible for the pathogen strain-specific transcriptomic response. Upon elt-2 knockdown worms exposed to MYBT18679 display lower survival rate coupled with higher intestinal damage than non-infected controls. Additionally, by performing further genetic analysis using gene knockdown and knockout, we found that the p38 MAPK pathway acts likely in parallel to elt-2 and the transcription factor skn-1 cooperates with elt-2 to promote resistance to MYBT18679. On the other hand, elt-2 knockdown leads to a substantially higher survival rate, together with lower intestinal tissue damage compared to control worms, upon exposure to MYBT18247, another pathogenic Bacillus thuringiensis strain. The MYBT18247 pathogen load of elt-2(RNAi) worms compared to control worms remained unchanged, suggesting the elt-2 negatively regulates tolerance towards MYBT18247. We found that tolerance to MYBT18247 was positively regulated by the transcription factors: FOXO daf-16, bZip zip-2, nhr-99 and nhr-193. To identify elt-2 negatively-regulated downstream targets that could promote tolerance to MYBT18247, we performed a second RNA-Seq experiment, this time including elt-2(RNAi) worms exposed to both pathogenic strains. We found four genes negatively regulated by elt-2: cdr-2, poml-3, dhs-30 and tre-3, with putative function in detoxification and lipid metabolism, which can mediate tolerance to MYBT18247. We conclude that ELT-2 coordinates strain-specific immune responses in this invertebrate host and promotes resistance upon exposure to MYBT18679, while it negatively regulates tolerance to MYBT18247. The response is likely to be specific to the crystal pore-forming toxins produced by this pathogen.

Dataset Information

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

Publications

Transcriptome Analysis of the Nematode <i>Caenorhabditis elegans</i> in Acidic Stress Environments.

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