Computational exploration of the genomic assignments, molecular structure, and dynamics of the ccdAB^Xn2 toxin-antitoxin homolog with its bacterial target, the DNA gyrase, in the entomopathogen Xenorhabdus nematophila

References

• An, R., & Grewal, P. S. (2016). Comparative analysis of Xenorhabdus koppenhoeferi gene expression during symbiotic persistence in the host nematode. PLoS ONE, 11(1), e0145739. In https://doi.org/10.1371/journal.pone.0145739
   PubMed Web of Science ®Google Scholar
• Awori, R. M. (2022). Nematophilic bacteria associated with entomopathogenic nematodes and drug development of their biomolecules. Frontiers in Microbiology, 13, 993688. https://doi.org/10.3389/FMICB.2022.993688
   PubMed Web of Science ®Google Scholar
• Babicki, S., Arndt, D., Marcu, A., Liang, Y., Grant, J. R., Maciejewski, A., & Wishart, D. S. (2016). Heatmapper: Web-enabled heat mapping for all. Nucleic Acids Research, 44(W1), W147–W153. https://doi.org/10.1093/NAR/GKW419
   PubMed Web of Science ®Google Scholar
• Bernard, P., & Couturier, M. (1992). Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. Journal of Molecular Biology, 226(3), 735–745. https://doi.org/10.1016/0022-2836(92)90629-X
   PubMed Web of Science ®Google Scholar
• Bode, E., He, Y., Vo, T. D., Schultz, R., Kaiser, M., & Bode, H. B. (2017). Biosynthesis and function of simple amides in Xenorhabdus doucetiae. Environmental Microbiology, 19(11), 4564–4575. https://doi.org/10.1111/1462-2920.13919
   PubMed Web of Science ®Google Scholar
• Boss, L., Górniak, M., Lewańczyk, A., Morcinek-Orłowska, J., Barańska, S., & Szalewska-Pałasz, A. (2021). Identification of three type II toxin-antitoxin systems in model bacterial plant pathogen Dickeya dadantii 3937. International Journal of Molecular Sciences, 22(11), 5932. https://doi.org/10.3390/IJMS22115932
   PubMed Web of Science ®Google Scholar
• Brachmann, A. O., Reimer, D., Lorenzen, W., Alonso, E. A., Kopp, Y., Piel, J., & Bode, H. B. (2013). Angewandte reciprocal cross talk between fatty acid and antibiotic biosynthesis in a nematode symbiont **. Angewandte Chemie (International ed. in English), 51(48), 12086–12089. https://doi.org/10.1002/anie.201205384
   Web of Science ®Google Scholar
• Bustamante, P., Tello, M., Orellana, O., & Hayes, F. (2014). Toxin-antitoxin systems in the mobile genome of Acidithiobacillus ferrooxidans. PloS One, 9(11), e112226. https://doi.org/10.1371/journal.pone.0112226
   PubMed Web of Science ®Google Scholar
• Cao, M., Patel, T., Rickman, T., Goodrich-Blair, H., & Hussa, E. A. (2017). High Levels of the Xenorhabdus nematophila transcription factor Lrp promote mutualism with the Steinernema carpocapsae nematode host. Applied and Environmental Microbiology, 83(12), e00276-17. https://doi.org/10.1128/AEM.00276-17
   Web of Science ®Google Scholar
• Chaston, J. M., Suen, G., Tucker, S. L., Andersen, A. W., Bhasin, A., Bode, E., Bode, H. B., Brachmann, A. O., Cowles, C. E., Cowles, K. N., Darby, C., de Léon, L., Drace, K., Du, Z., Givaudan, A., Herbert Tran, E. E., Jewell, K. A., Knack, J. J., Krasomil-Osterfeld, K. C., … Goodrich-Blair, H. (2011). The entomopathogenic bacterial Endosymbionts xenorhabdus and photorhabdus: Convergent lifestyles from divergent genomes. PloS One, 6(11), e27909. https://doi.org/10.1371/journal.pone.0027909
   PubMed Web of Science ®Google Scholar
• Chaudhary, S., Singh, G., Gupta, N., Ghosh, C., & Rathore, J. S. (2023). New face in the row of bioactive compounds and toxin-antitoxin modules: Xenorhabdus nematophila. Journal of Asia-Pacific Entomology, 26(4), 102148. https://doi.org/10.1016/j.aspen.2023.102148
   Web of Science ®Google Scholar
• Chaudhary, S., Yadav, M., Mathpal, S., Chandra, S., & Rathore, J. S. (2023). Genomic assortment and interactive insights of the chromosomal encoded control of cell death (CCD) toxin-antitoxin (TA) module in Xenorhabdus nematophila. Journal of Biomolecular Structure & Dynamics, 41(15), 7032–7044. https://doi.org/10.1080/07391102.2022.2114940
   PubMed Web of Science ®Google Scholar
• Christensen, S. K., Pedersen, K., Hansen, F. G., & Gerdes, K. (2003). Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. Journal of Molecular Biology, 332(4), 809–819. https://doi.org/10.1016/S0022-2836(03)00922-7
   PubMed Web of Science ®Google Scholar
• Di Cesare, A., Losasso, C., Barco, L., Eckert, E. M., Conficoni, D., Sarasini, G., Corno, G., & Ricci, A. (2016). Diverse distribution of Toxin-Antitoxin II systems in Salmonella enterica serovars. Scientific Reports, 20166(1), 28759. 6(1 https://doi.org/10.1038/srep28759
   Google Scholar
• Dreyer, J., Malan, A. P., & Dicks, L. M. T. (2018). Bacteria of the genus Xenorhabdus, a novel source of bioactive compounds. Frontiers in Microbiology, 9(December), 3177. https://doi.org/10.3389/fmicb.2018.03177
   PubMedGoogle Scholar
• Forst, S., Dowds, B., Boemare, N., & Stackebrandt, E. (1997). XENORHABDUS AND PHOTORHABDUS SPP.: Bugs that kill bugs. Annual Review of Microbiology, 51, 47–72. https://doi.org/10.1146/annurev.micro.51.1.47
   PubMed Web of Science ®Google Scholar
• Fukruksa, C., Yimthin, T., Suwannaroj, M., Muangpat, P., Tandhavanant, S., Thanwisai, A., & Vitta, A. (2017). Isolation and identification of Xenorhabdus and Photorhabdus bacteria associated with entomopathogenic nematodes and their larvicidal activity against Aedes aegypti. Parasites & Vectors, 10(1), 1–10. https://doi.org/10.1186/s13071-017-2383-2
   PubMedGoogle Scholar
• Gautam, L. K., Yadav, M., & Rathore, J. S. (2017). Functional annotation of a novel toxin – antitoxin system Xn-Relt of xenorhabdus nematophila ; a combined in silico and in vitro approach. Journal of Molecular Modeling, 23(6), 1–9. https://doi.org/10.1007/s00894-017-3361-5
   Google Scholar
• Germe, T., Vörös, J., Jeannot, F., Taillier, T., Stavenger, R. A., Bacqué, E., Maxwell, A., & Bax, B. D. (2018). A new class of antibacterials, the imidazopyrazinones, reveal structural transitions involved in DNA gyrase poisoning and mechanisms of resistance. Nucleic Acids Research, 46(8), 4114–4128. https://doi.org/10.1093/NAR/GKY181
   PubMed Web of Science ®Google Scholar
• Gupta, K., Tripathi, A., Sahu, A., & Varadarajan, R. (2017). Contribution of the chromosomal ccdAB operon to bacterial drug tolerance. Journal of Bacteriology, 199(19), e00397-17. https://doi.org/10.1128/JB.00397-17
   Web of Science ®Google Scholar
• Hallez, R., Geeraerts, D., Sterckx, Y., Mine, N., Loris, R., & Van Melderen, L. (2010). New toxins homologous to ParE belonging to three-component toxin-antitoxin systems in Escherichia coli O157:H7. Molecular Microbiology, 76(3), 719–732. https://doi.org/10.1111/j.1365-2958.2010.07129.x
   PubMed Web of Science ®Google Scholar
• Harms, A., Brodersen, D. E., Mitarai, N., & Gerdes, K. (2018). Toxins, targets, and triggers: An overview of toxin-antitoxin biology. Molecular Cell, 70(5), 768–784. https://doi.org/10.1016/j.molcel.2018.01.003
   PubMed Web of Science ®Google Scholar
• Hussa, E. A., Casanova-Torres, Á. M., & Goodrich-Blair, H. (2015). The Global Transcription Factor Lrp Controls Virulence Modulation in Xenorhabdus nematophila. Journal of Bacteriology, 197(18), 3015–3025. https://doi.org/10.1128/JB.00272-15
   PubMed Web of Science ®Google Scholar
• James, M., Malan, A. P., & Addison, P. (2018). Surveying and screening South African entomopathogenic nematodes for the control of the Mediterranean fruit fl y, Ceratitis capitata (Wiedemann). Crop Protection, 105(March 2018), 41–48. https://doi.org/10.1016/j.cropro.2017.11.008
   Google Scholar
• Jeannot, F., Taillier, T., Stavenger, R. A., Germe, T., Judit, V., Maxwell, A., Bax, B. D., & Bacqu, E. (2018). A new class of antibacterials, the imidazopyrazinones, reveal structural transitions involved in DNA gyrase poisoning and mechanisms of resistance. https://doi.org/10.1093/nar/gky181
   Google Scholar
• Kamruzzaman, M., Wu, A. Y., & Iredell, J. R. (2021). Biological functions of type II toxin-antitoxin systems in bacteria. Microorganisms, 9(6), 1276. https://doi.org/10.3390/MICROORGANISMS9061276
   PubMed Web of Science ®Google Scholar
• Kozakov, D., Hall, D. R., Xia, B., Porter, K. A., Padhorny, D., Yueh, C., Beglov, D., & Vajda, S. (2017). The ClusPro web server for protein-protein docking. Nature Protocols, 12(2), 255–278. https://doi.org/10.1038/NPROT.2016.169
   PubMed Web of Science ®Google Scholar
• Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J., & Marra, M. A. (2009). Circos: An information aesthetic for comparative genomics. Genome Research, 19(9), 1639–1645. https://doi.org/10.1101/gr.092759.109
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51(10), 2778–2786. https://doi.org/10.1021/CI200227U/ASSET/IMAGES/MEDIUM/CI-2011-00227U_0006.GIF
   PubMed Web of Science ®Google Scholar
• Lawson, D. M., Buttner, M. J., Sch, M., & Maxwell, A. (2018). Structural insights into simocyclinone as an antibiotic, effector ligand and substrate. FEMS Microbiology Reviews, 42November 2017, (1), 100–112. https://doi.org/10.1093/femsre/fux055
   Web of Science ®Google Scholar
• Lefoulon, E., McMullen, J. G., & Stock, S. P. (2022). Transcriptomic analysis of steinernema nematodes highlights metabolic costs associated to Xenorhabdus endosymbiont association and rearing conditions. Frontiers in Physiology, 13(February), 821845. https://doi.org/10.3389/fphys.2022.821845
   PubMedGoogle Scholar
• Lucas, J., Goetsch, M., Fischer, M., & Forst, S. (2018). Characterization of the pixB gene in Xenorhabdus nematophila and discovery of a new gene family. Microbiology (Reading, England), 164(4), 495–508. https://doi.org/10.1099/mic.0.000626
   PubMed Web of Science ®Google Scholar
• Martens, E. C., Heungens, K., & Goodrich-Blair, H. (2003). Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. Journal of Bacteriology, 185(10), 3147–3154. https://doi.org/10.1128/JB.185.10.3147-3154.2003
   PubMed Web of Science ®Google Scholar
• Ogura, T., & Hiraga, S. (1983). Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proceedings of the National Academy of Sciences of the United States of America, 80(15), 4784–4788. https://doi.org/10.1073/pnas.80.15.4784
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera?A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., Van Der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/BIOINFORMATICS/BTT055
   PubMed Web of Science ®Google Scholar
• Rathore, J. S., & Gautam, L. K. (2014). Expression, purification, and functional analysis of novel RelE operon from X. nematophila. TheScientificWorldJournal, 2014, 428159–428157. https://doi.org/10.1155/2014/428159
   PubMedGoogle Scholar
• Richards, G. R., & Goodrich-Blair, H. (2009). Masters of conquest and pillage: Xenorhabdus nematophila global regulators control transitions from virulence to nutrient acquisition. Cellular Microbiology, 11(7), 1025–1033. https://doi.org/10.1111/J.1462-5822.2009.01322.X
   PubMed Web of Science ®Google Scholar
• Robert, X., & Gouet, P. (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42(Web Server issue), W320–W324. https://doi.org/10.1093/nar/gku316
   PubMed Web of Science ®Google Scholar
• Sajnaga, E., & Kazimierczak, W. (2020). Evolution and taxonomy of nematode-associated entomopathogenic bacteria of the genera Xenorhabdus and Photorhabdus : An overview. Symbiosis, 80(1), 1–13. https://doi.org/10.1007/s13199-019-00660-0
   Web of Science ®Google Scholar
• Salentin, S., Schreiber, S., Haupt, V. J., Adasme, M. F., & Schroeder, M. (2015). PLIP: fully automated protein–ligand interaction profiler. Nucleic Acids Research, 43(W1), W443–W447. https://doi.org/10.1093/nar/gkv315
   PubMed Web of Science ®Google Scholar
• Sevin, E. W., & Barloy-Hubler, F. (2007). RASTA-Bacteria: a web-based tool for identifying toxin-antitoxin loci in prokaryotes. Genome Biology, 8(8), R155.1–14. https://doi.org/10.1186/gb-2007-8-8-r155
   Web of Science ®Google Scholar
• Shao, Y., Harrison, E. M., Bi, D., Tai, C., He, X., Ou, H. Y., Rajakumar, K., & Deng, Z. (2011). TADB: a web-based resource for Type 2 toxin-antitoxin loci in bacteria and archaea. Nucleic Acids Research, 39(Database issue), D606–D611. https://doi.org/10.1093/NAR/GKQ908
   PubMedGoogle Scholar
• Singh, G., Yadav, M., Ghosh, C., & Rathore, J. S. (2021). Bacterial toxin-antitoxin modules: Classification, functions, and association with persistence. Current Research in Microbial Sciences, 2, 100047. https://doi.org/10.1016/J.CRMICR.2021.100047
   PubMedGoogle Scholar
• Singh, J., & Banerjee, N. (2008). Transcriptional analysis and functional characterization of a gene pair encoding iron-regulated xenocin and immunity proteins of Xenorhabdus nematophila. Journal of Bacteriology, 190(11), 3877–3885. https://doi.org/10.1128/JB.00209-08
   PubMed Web of Science ®Google Scholar
• Stilwell, M. D., Cao, M., Goodrich-Blair, H., & Weibel, D. B. (2018). Studying the symbiotic bacterium Xenorhabdus nematophila in individual, living Steinernema carpocapsae nematodes using microfluidic systems. mSphere, 3(1), 1–16. https://doi.org/10.1128/mSphere.00530-17
   PubMedGoogle Scholar
• Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., Jensen, L. J., & Mering, C. V (2018). STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research, 47(D1), D607–D613. https://doi.org/10.1093/nar/gky1131
   Web of Science ®Google Scholar
• Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/MOLBEV/MSAB120
   PubMed Web of Science ®Google Scholar
• Thompson, J. D., Higgins, +, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC308517/pdf/nar00046-0131.pdf https://doi.org/10.1093/nar/22.22.4673
   PubMed Web of Science ®Google Scholar
• Tripathi, A., Dewan, P. C., Barua, B., & Varadarajan, R. (2012). Additional role for the CCD operon of F-plasmid as a transmissible persistence factor. Proceedings of the National Academy of Sciences of the United States of America, 109(31), 12497–12502. https://doi.org/10.1073/PNAS.1121217109/SUPPL_FILE/PNAS.201121217SI.PDF
   PubMed Web of Science ®Google Scholar
• Van Der Hooft, J. J. J., Goldstone, R. J., Harris, S., Burgess, K. E. V., & Smith, D. G. E. (2019). Substantial extracellular metabolic differences found between phylogenetically closely related probiotic and pathogenic strains of Escherichia coli. Frontiers in Microbiology, 10(FEB), 252. https://doi.org/10.3389/FMICB.2019.00252/BIBTEX
   PubMedGoogle Scholar
• Van Melderen, L., Bernard, P., & Couturier, M. (1994). Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Molecular Microbiology, 11(6), 1151–1157. https://doi.org/10.1111/J.1365-2958.1994.TB00391.X
   PubMed Web of Science ®Google Scholar
• Vandervelde, A., Drobnak, I., Hadži, S., Sterckx, Y. G.-J., Welte, T., De Greve, H., Charlier, D., Efremov, R., Loris, R., & Lah, J. (2017). NAR Breakthrough Article Molecular mechanism governing ratio-dependent transcription regulation in the ccdAB operon. Nucleic Acids Research, 45(6), 2937–2950. https://doi.org/10.1093/nar/gkx108
   PubMed Web of Science ®Google Scholar
• Wang, Y. H., Feng, J. T., Zhang, Q., & Zhang, X. (2008). Optimization of fermentation condition for antibiotic production by Xenorhabdus nematophila with response surface methodology. Journal of Applied Microbiology, 104(3), 735–744. https://doi.org/10.1111/j.1365-2672.2007.03599.x
   PubMed Web of Science ®Google Scholar
• Xu, J., Xia, K., Li, P., Qian, C., Li, Y., & Liang, X. (2020). Functional investigation of the chromosomal ccdAB and hipAB operon in Escherichia coli Nissle 1917. Applied Microbiology and Biotechnology, 104(15), 6731–6747. https://doi.org/10.1007/S00253-020-10733-6
   PubMedGoogle Scholar
• Yadav, M., & Rathore, J. S. (2018). TAome analysis of type-II toxin-antitoxin system from Xenorhabdus nematophila. Computational Biology and Chemistry, 76, 293–301. https://doi.org/10.1016/j.compbiolchem.2018.07.010
   PubMed Web of Science ®Google Scholar
• Yadav, M., Sarkar, S., Olymon, K., Ray, S. K., & Kumar, A. (2023). Combined In Silico and In Vitro Study to Reveal the Structural Insights and Nucleotide-Binding Ability of the Transcriptional Regulator PehR from the Phytopathogen Ralstonia solanacearum. ACS Omega, 8(38), 34499–34515. https://doi.org/10.1021/ACSOMEGA.3C03175
   PubMed Web of Science ®Google Scholar
• Yang, J., & Zhang, Y. (2015). I-TASSER server: New development for protein structure and function predictions. Web Server Issue Published Online, 43. Nucleic Acids Research, 43(W1), W174–W181.
   Google Scholar
• Yang, J., Roy, A., & Zhang, Y. (2013). Protein–ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment. Bioinformatics, 29(20), 2588–2595. https://doi.org/10.1093/bioinformatics/btt447
   PubMed Web of Science ®Google Scholar
• Zheng, W., Zhang, C., Wuyun, Q., Pearce, R., Li, Y., & Zhang, Y. (2019). LOMET S2: improved meta-threading server for fold-recognition and structure-based function annotation for distant-homology proteins. Nucleic Acids Research, 47, 429–436. https://doi.org/10.1093/nar/gkz384
   PubMed Web of Science ®Google Scholar