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A Proteomic Analysis Provides Novel Insights into the Stress Responses of Caenorhabditis elegans towards Nematicidal Cry6A Toxin from Bacillus thuringiensis.

ABSTRACT: Cry6A represents a novel family of nematicidal crystal proteins from Bacillus thuringiensis. It has distinctive architecture as well as mechanism of action from Cry5B, a highly focused family of nematicidal crystal proteins, and even from other insecticidal crystal proteins containing the conserved three-domain. However, how nematode defends against Cry6A toxin remains obscure. In this study, the global defense pattern of Caenorhabditis elegans against Cry6Aa2 toxin was investigated by proteomic analysis. In response to Cry6Aa2, 12 proteins with significantly altered abundances were observed from worms, participating in innate immune defense, insulin-like receptor (ILR) signaling pathway, energy metabolism, and muscle assembly. The differentially expressed proteins (DEPs) functioning in diverse biological processes suggest that a variety of defense responses participate in the stress responses of C. elegans to Cry6Aa2. The functional verifications of DEPs suggest that ILR signaling pathway, DIM-1, galectin LEC-6 all are the factors of defense responses to Cry6Aa2. Moreover, Cry6Aa2 also involves in accelerating the metabolic energy production which fulfills the energy demand for the immune responses. In brief, our findings illustrate the global pattern of defense responses of nematode against Cry6A for the first time, and provide a novel insight into the mechanism through which worms respond to Cry6A.

SUBMITTER: Wang B

PROVIDER: S-EPMC5658354 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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A Proteomic Analysis Provides Novel Insights into the Stress Responses of Caenorhabditis elegans towards Nematicidal Cry6A Toxin from Bacillus thuringiensis.

Wang Bing B Wang Haiwen H Xiong Jing J Zhou Qiaoni Q Wu Huan H Xia Liqiu L Li Lin L Yu Ziquan Z

Scientific reports 20171026 1

Cry6A represents a novel family of nematicidal crystal proteins from Bacillus thuringiensis. It has distinctive architecture as well as mechanism of action from Cry5B, a highly focused family of nematicidal crystal proteins, and even from other insecticidal crystal proteins containing the conserved three-domain. However, how nematode defends against Cry6A toxin remains obscure. In this study, the global defense pattern of Caenorhabditis elegans against Cry6Aa2 toxin was investigated by proteomic ...[more]

PMID: 29074967

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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

A Proteomic Analysis Provides Novel Insights into the Stress Responses of Caenorhabditis elegans towards Nematicidal Cry6A Toxin from Bacillus thuringiensis.

Publications

A Proteomic Analysis Provides Novel Insights into the Stress Responses of Caenorhabditis elegans towards Nematicidal Cry6A Toxin from Bacillus thuringiensis.

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