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Proteomic analysis of Caenorhabditis elegans against Salmonella Typhi toxic proteins

Genes & Immunity volume 22, pages 75–92 (2021)Cite this article

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Abstract

Bacterial effector molecules are crucial infectious agents that can cause pathogenesis. In the present study, the pathogenesis of toxic Salmonella enterica serovar Typhi (S. Typhi) proteins on the model host Caenorhabditis elegans was investigated by exploring the host’s regulatory proteins during infection through the quantitative proteomics approach. Extracted host proteins were analyzed using two-dimensional gel electrophoresis (2D-GE) and differentially regulated proteins were identified using MALDI TOF/TOF/MS analysis. Of the 150 regulated proteins identified, 95 were downregulated while 55 were upregulated. The interaction network of regulated proteins was predicted using the STRING tool. Most downregulated proteins were involved in muscle contraction, locomotion, energy hydrolysis, lipid synthesis, serine/threonine kinase activity, oxidoreductase activity, and protein unfolding. Upregulated proteins were involved in oxidative stress pathways. Hence, cellular stress generated by S. Typhi proteins in the model host was determined using lipid peroxidation as well as oxidant and antioxidant assays. In addition, candidate proteins identified via extract analysis were validated by western blotting, and the roles of several crucial molecules were analyzed in vivo using transgenic strains (myo-2 and col-19) and mutant (ogt-1) of C. elegans. To the best of our knowledge, this is the first study to report protein regulation in host C. elegans exposed to toxic S. Typhi proteins. It highlights the significance of p38 MAPK and JNK immune pathways.

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Fig. 1: Graph represents the survival of C. elegans during extracted protein exposure.
Fig. 2: 2D gel electrophoreses images of C. elegans proteome.
Fig. 3: Analysis of Gene Ontology categories.
Fig. 4: Interactome map using the STRING tool with a medium confidence score (0.400), revealing an interaction between identified protein players which were regulated by 50% S. Typhi toxin protein exposure in C. elegans.
Fig. 5: Functional annotations and protein enrichment score of regulated proteins.
Fig. 6: Quantitative analysis of oxidant and antioxidant proteins of C. elegans fed with E. coli OP50 and treated with S. Typhi toxin proteins and E. coli OP50 total proteins.
Fig. 7: Expression of MAP Kinase pathway proteins.
Fig. 8: Impact of toxin proteins on host fat molecules.
Fig. 9: Impact of toxin proteins on the ATP production.
Fig. 10: Impact of toxin proteins on host locomotion.
Fig. 11: An overview of proteins and pathways activated and targeted by S. Typhi toxin in C. elegans are presented in this figure.

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Acknowledgements

We thank the Caenorhabditis Genetics Centre, which is funded by the National Institute of Health, National Centre for Research Resources for providing the nematode strains. DAM gratefully acknowledges the University Grants Commission (UGC) of India for the financial assistance in the form of UGC-PF (F. No. 42–222/2013 (SR)). The computational facility provided by the Bioinformatics Infrastructure Facility, Alagappa University funded by the Department of Biotechnology, Ministry of Science and Technology, Government of India (Grant No.BT/BI/25/015/2012 (BIF)) are thankfully acknowledged. We are also grateful for the Instrumentation Facility provided by the Department of Science and Technology (DST), Government of India through DST PURSE [Grant No. SR/S9Z-415 23/2010/42(G)], DST FIST [Grant No.SR-FST/LSI-087/2008], UGC through SAP-DRS1 [Grant No. F. 3–28/2011(SAP-II)] and RUSA 2.0. [F. 24–51/2014-U, Policy (TN Multi-Gen), Dept. of Education, GOI].

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  1. Department of Biotechnology, Alagappa University, Karaikudi, Tamil Nadu, India

    Dilawar Ahmad Mir, Boopathi Balasubramaniam, Lappasi Mohanram VenkataKrishna, Balasubramanian Chellammal Muthubharathi & Krishnaswamy Balamurugan

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DAM, BB and MB designed and performed the experiments and analysed the data. VK helped in proteomic analysis. KB wrote the manuscript in consultation with DAM and other authors.

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Correspondence to Krishnaswamy Balamurugan.

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Mir, D.A., Balasubramaniam, B., VenkataKrishna, L.M. et al. Proteomic analysis of Caenorhabditis elegans against Salmonella Typhi toxic proteins. Genes Immun 22, 75–92 (2021). https://doi.org/10.1038/s41435-021-00132-w

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