Pathogen-induced dormancy in liquid limits gastrointestinal colonization of Caenorhabditis elegans

References

• Septimus EJ. Antimicrobial resistance: an antimicrobial/diagnostic stewardship and infection prevention approach. Med Clin North Am. 2018;102(5):819–15.
   PubMed Web of Science ®Google Scholar
• Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74(3):417–433.
   PubMed Web of Science ®Google Scholar
• Munita JM, Arias CA, Kudva IT. Mechanisms of antibiotic resistance. Microbiol Spectr. 2016;4(2). DOI:10.1128/microbiolspec.VMBF-0016-2015
   PubMed Web of Science ®Google Scholar
• CDC. Antibiotic resistance threats in the United States, 2019. Atlanta, GA: U.S.: Department of Health and Human Services; 2019p 145.
   Google Scholar
• Pang Z, Raudonis R, Glick BR, et al. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv. 2019;37(1):177–192.
   PubMed Web of Science ®Google Scholar
• Gellatly SL, Hancock RE. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis. 2013;67(3):159–173.
   PubMed Web of Science ®Google Scholar
• Jurado-Martin I, Sainz-Mejias M, McClean S. Pseudomonas aeruginosa: an audacious pathogen with an adaptable arsenal of virulence factors. Int J Mol Sci. 2021;22(6):3128.
   PubMed Web of Science ®Google Scholar
• Conradt B, Claycomb MJGBSKOKD A, Colon-Ramos DA, et al. The power of C. elegans: a tribute to Sydney brenner. Dev Cell. 2019;49(4):496–498.
   PubMed Web of Science ®Google Scholar
• Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94.
   PubMed Web of Science ®Google Scholar
• TM MMS, Rahme LG, Ausubel FM. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell. 1999;96(1):10.
   Web of Science ®Google Scholar
• Kim DH, Ewbank JJ. Signaling in the innate immune response. WormBook. 2018;2018:1–35.
   PubMedGoogle Scholar
• Sorathia N, Rajadhyaksha MS. Caenorhabditis elegans: a model for studying human pathogen biology. Recent Pat Biotechnol. 2016;10(2):217–225.
   PubMedGoogle Scholar
• Marsh EK, May RC. Caenorhabditis elegans, a model organism for investigating immunity. Appl Environ Microbiol. 2012;78(7):2075–2081.
   PubMed Web of Science ®Google Scholar
• Utari PD, Quax WJ. Caenorhabditis elegans reveals novel Pseudomonas aeruginosa virulence mechanism. Trends Microbiol. 2013;21(7):315–316.
   PubMed Web of Science ®Google Scholar
• Kirienko NV, Kirienko DR, Larkins-Ford J, et al. Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death. Cell Host Microbe. 2013;13(4):406–416.
   PubMed Web of Science ®Google Scholar
• Anderson QL, Revtovich AV, Kirienko NAHT, et al. A High-throughput, High-content, Liquid-based C. elegans Pathosystem Elegans Pathosystem. J Vis Exp. 2018;2018(137). DOI:10.3791/58068
   Google Scholar
• Pukkila-Worley R, Peleg AY, Tampakakis E, et al. Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot Cell. 2009;8(11):1750–1758.
   PubMed Web of Science ®Google Scholar
• Moy TI, Ball AR, Anklesaria Z, et al. Identification of novel antimicrobials using a live-animal infection model. Proc Natl Acad Sci U S A. 2006;103(27):10414–10419.
   PubMed Web of Science ®Google Scholar
• Ben-Yakar A, Bourgeois F. Ultrafast laser nanosurgery in microfluidics for genome-wide screenings. Curr Opin Biotechnol. 2009;20(1):100–105.
   PubMed Web of Science ®Google Scholar
• Giunti S, Andersen N, Rayes D, et al. Drug discovery: insights from the invertebrate Caenorhabditis elegans. Pharmacol Res Perspect. 2021;9(2):e00721.
   PubMed Web of Science ®Google Scholar
• Kang D, Kirienko NV. High-throughput genetic screen reveals that early attachment and biofilm formation are necessary for full pyoverdine production by Pseudomonas aeruginosa. Front Microbiol. 2017;8:1707.
   PubMed Web of Science ®Google Scholar
• Kirienko DR, Revtovich AV, High-Content KNA. Phenotypic screen identifies fluorouridine as an inhibitor of pyoverdine biosynthesis and pseudomonas aeruginosa virulence. mSphere. 2016;1(4). DOI:10.1128/mSphere.00217-16
   PubMed Web of Science ®Google Scholar
• Jiang H, Wang D. The microbial zoo in the c. elegans intestine: bacteria, fungi and viruses. Viruses. 2018;10(2). DOI:10.3390/v10020085
   Web of Science ®Google Scholar
• Schulenburg H, Ewbank JJ. The genetics of pathogen avoidance in Caenorhabditis elegans. Mol Microbiol. 2007;66(3):563–570.
   PubMed Web of Science ®Google Scholar
• Cohen LB, Troemel ER. Microbial pathogenesis and host defense in the nematode C. elegans. Curr Opin Microbiol. 2015;23:94–101.
   PubMed Web of Science ®Google Scholar
• Wang Y, Ezemaduka AN, Tang Y, et al. Understanding the mechanism of the dormant dauer formation of C. elegans: from genetics to biochemistry. IUBMB Life. 2009;61(6):607–612.
   PubMed Web of Science ®Google Scholar
• Hill AJ, Mansfield R, Lopez JM, et al. Cellular stress induces a protective sleep-like state in C. elegans. Curr Biol. 2014;24(20):2399–2405.
   PubMed Web of Science ®Google Scholar
• Nath RD, Chow ES, Wang H, et al. Elegans stress-induced sleep emerges from the collective action of multiple neuropeptides. Curr Biol. 2016;26(18):2446–2455.
   PubMed Web of Science ®Google Scholar
• Fire A, Xu S, Montgomery MK, et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806–811.
   PubMed Web of Science ®Google Scholar
• Beanan MJ, Strome S. Characterization of a germ-line proliferation mutation in C. elegans. Development. 1992;116(3):755–766.
   PubMed Web of Science ®Google Scholar
• Dunbar TL, Yan Z, Balla KM, et al. Elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell Host Microbe. 2012;11(4):375–386.
   PubMed Web of Science ®Google Scholar
• Kirienko NV, Cezairliyan BO, Ausubel FM, et al. Pseudomonas aeruginosa PA14 pathogenesis in Caenorhabditis elegans. Methods Mol Biol. 2014;1149:653–669.
   PubMedGoogle Scholar
• Zhang L, Tan FC, Strasfeld L, et al. Long-term dominance of carbapenem-non-susceptible pseudomonas aeruginosa ST111 in hematologic malignancy patients and hematopoietic cell transplant recipients. Front Cell Infect Microbiol. 2022;12:904602.
   PubMed Web of Science ®Google Scholar
• Garsin DA, Sifri CD, Mylonakis E, et al. A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A. 2001;98(19):10892–10897. DOI:10.1073/pnas.191378698
   PubMed Web of Science ®Google Scholar
• Mahajan-Miklos S, Tan MW, Rahme LG, et al. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell. 1999;96(1):47–56.
   PubMed Web of Science ®Google Scholar
• Sifri CD, Begun J, Ausubel FM, et al. Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun. 2003;71(4):2208–2217.
   PubMed Web of Science ®Google Scholar
• Gerstbrein B, Stamatas G, Kollias N, et al. In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell. 2005;4(3):127–137.
   PubMed Web of Science ®Google Scholar
• Komura T, Yamanaka M, Nishimura K, et al. Autofluorescence as a noninvasive biomarker of senescence and advanced glycation end products in Caenorhabditis elegans. NP J Aging Mech Dis. 2021;7(1):12.
   PubMed Web of Science ®Google Scholar
• Pincus Z, Mazer TC, Slack FJ. Autofluorescence as a measure of senescence in C. elegans: look to red, not blue or green. Aging (Albany NY). 2016;8(5):889–898.
   PubMedGoogle Scholar
• Teuscher AC, Ewald CY. Overcoming Autofluorescence to Assess GFP Expression During Normal Physiology and Aging in Caenorhabditis elegans. Bio Protoc. 2018;8(14). DOI:10.21769/BioProtoc.2940
   PubMedGoogle Scholar
• Ibanez-Ventoso C, Herrera C, Chen E, et al. Automated Analysis of C. elegans Swim Behavior Using CeleST Software. J Vis Exp. 2016;2016(118). DOI:10.3791/54359-v
   Google Scholar
• Rosiana S, Zhang L, Kim GH, et al. Comprehensive genetic analysis of adhesin proteins and their role in virulence of Candida albicans. Genetics. 2021;217(2).
   PubMed Web of Science ®Google Scholar
• Craig L, Forest KT, Maier B. Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol. 2019;17(7):429–440.
   PubMed Web of Science ®Google Scholar
• Thi MTT, Wibowo D, Rehm BHA. Pseudomonas aeruginosa Biofilms. Int J Mol Sci. 2020;21(22):8671.
   PubMed Web of Science ®Google Scholar
• Landi A, Mari M, Kleiser S, et al. Pseudomonas aeruginosa lectin LecB impairs keratinocyte fitness by abrogating growth factor signalling. Life Sci Alliance. 2019;2(6):e201900422. DOI:10.26508/lsa.201900422
   PubMed Web of Science ®Google Scholar
• Marmont LS, Whitfield GB, Rich JD, et al. PelA and PelB proteins form a modification and secretion complex essential for Pel polysaccharide-dependent biofilm formation in Pseudomonas aeruginosa. J Biol Chem. 2017;292(47):19411–19422. DOI:10.1074/jbc.M117.812842
   PubMed Web of Science ®Google Scholar
• Kang D, Turner KE, Kirienko NV. PqsA Promotes Pyoverdine Production via Biofilm Formation. Pathogens. 2017;7(1). DOI:10.3390/pathogens7010003
   PubMed Web of Science ®Google Scholar
• Celen I, Doh JH, Sabanayagam CR. Effects of liquid cultivation on gene expression and phenotype of C. elegans. BMC Genomics. 2018;19(1):562.
   PubMedGoogle Scholar
• Kirienko NV, Ausubel FM, Ruvkun G Mitophagy confers resistance to siderophore-mediated killing by Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(6):1821–1826.
   Google Scholar
• Comerlato CB, Resende MC, Caierao J, et al. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Mem Inst Oswaldo Cruz. 2013;108(5):590–595.
   PubMed Web of Science ®Google Scholar
• Soto R, Goetting DL, Van Buskirk C. NPR-1 Modulates Plasticity in C. elegans Stress-Induced Sleep. iScience. 2019;19:1037–1047.
   PubMed Web of Science ®Google Scholar
• Kang D, Zhang L, Kirienko NV. High-Throughput Approaches for the Identification of Pseudomonas aeruginosa Antivirulents. MBio. 2021;12(3). DOI:10.1128/mBio.02240-20
   Web of Science ®Google Scholar
• Cai X, Zheng W, Li Z. High-Throughput Screening Strategies for the Development of Anti-Virulence Inhibitors Against Staphylococcus aureus. Curr Med Chem. 2019;26(13):2297–2312.
   PubMed Web of Science ®Google Scholar
• Skariyachan S, Taskeen N, Ganta M, et al. Recent perspectives on the virulent factors and treatment options for multidrug-resistant Acinetobacter baumannii. Crit Rev Microbiol. 2019;45(3):315–333.
   PubMed Web of Science ®Google Scholar
• Breger J, Fuchs BB, Aperis G, et al. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLOS Pathog. 2007;3(2):e18.
   PubMed Web of Science ®Google Scholar
• Moy TI, Conery AL, Larkins-Ford J, et al. High-throughput screen for novel antimicrobials using a whole animal infection model. ACS Chem Biol. 2009;4(7):527–533. DOI:10.1021/cb900084v
   PubMed Web of Science ®Google Scholar
• Laranjeiro R, Harinath G, Burke D, et al. Single swim sessions in C. elegans induce key features of mammalian exercise. BMC Biol. 2017;15(1):30.
   PubMedGoogle Scholar
• Jones D, Candido EP. Feeding is inhibited by sublethal concentrations of toxicants and by heat stress in the nematode Caenorhabditis elegans: relationship to the cellular stress response. J Exp Zool. 1999;284(2):147–157.
   PubMedGoogle Scholar
• Smith MP, Laws TR, Atkins TP, et al. A liquid-based method for the assessment of bacterial pathogenicity using the nematode Caenorhabditis elegans. FEMS Microbiol Lett. 2002;210(2):181–185.
   PubMed Web of Science ®Google Scholar
• Alper S, McBride SJ, Lackford B, et al. Specificity and complexity of the Caenorhabditis elegans innate immune response. Mol Cell Biol. 2007;27(15):5544–5553.
   PubMed Web of Science ®Google Scholar
• McEwan DL, Kirienko NV, Ausubel FM. Host translational inhibition by Pseudomonas aeruginosa Exotoxin a Triggers an immune response in Caenorhabditis elegans. Cell Host Microbe. 2012;11(4):364–374.
   PubMed Web of Science ®Google Scholar
• Tjahjono E, Kirienko NV. A conserved mitochondrial surveillance pathway is required for defense against Pseudomonas aeruginosa. PLoS Genet. 2017;13(6):e1006876.
   PubMed Web of Science ®Google Scholar
• Garsin DA, Villanueva JM, Begun J, et al. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science. 2003;300(5627):1921. DOI:10.1126/science.1080147
   PubMed Web of Science ®Google Scholar
• Revtovich AV, Tjahjono E, Singh KV, et al. Development and Characterization of High-Throughput Caenorhabditis elegans - Enterococcus faecium Infection Model. Front Cell Infect Microbiol. 2021;11:667327.
   PubMed Web of Science ®Google Scholar
• HJ L, JR K, DiDomenico B, et al. Albicans mutants are avirulent. Cell. 1997;90(5):939–949.
   PubMed Web of Science ®Google Scholar
• Chavez V, Mohri-Shiomi A, Garsin DA. Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect Immun. 2009;77(11):4983–4989.
   PubMed Web of Science ®Google Scholar
• Sifri CD, Mylonakis E, Singh KV, et al. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun. 2002;70(10):5647–5650. DOI:10.1128/IAI.70.10.5647-5650.2002
   PubMed Web of Science ®Google Scholar
• Tiller GR, Garsin DA. The SKPO-1 peroxidase functions in the hypodermis to protect Caenorhabditis elegans from bacterial infection. Genetics. 2014;197(2):515–526.
   PubMed Web of Science ®Google Scholar
• Trojanowski NF, Nelson MD, Flavell SW, et al. Distinct Mechanisms Underlie Quiescence during Two Caenorhabditis elegans Sleep-Like States. J Neurosci. 2015;35(43):14571–14584.
   PubMed Web of Science ®Google Scholar
• Sanders J, Nagy S, Fetterman G, et al. The Caenorhabditis elegans interneuron ALA is (also) a high-threshold mechanosensor. BMC Neurosci. 2013;14(1):156.
   PubMedGoogle Scholar
• Nelson MD, Lee KH, Churgin MA, et al. Fmrfamide-like FLP-13 neuropeptides promote quiescence following heat stress in Caenorhabditis elegans. Curr Biol. 2014;24(20):2406–2410. DOI:10.1016/j.cub.2014.08.037
   PubMed Web of Science ®Google Scholar