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Abstract

Though bacteriophages (phages) are known to play a crucial role in bacterial fitness and virulence, our knowledge about the genetic basis of their interaction, cross-resistance and host-range is sparse. Here, we employed genome-wide screens in serovar Typhimurium to discover host determinants involved in resistance to eleven diverse lytic phages including four new phages isolated from a therapeutic phage cocktail. We uncovered 301 diverse host factors essential in phage infection, many of which are shared between multiple phages demonstrating potential cross-resistance mechanisms. We validate many of these novel findings and uncover the intricate interplay between RpoS, the virulence-associated general stress response sigma factor and RpoN, the nitrogen starvation sigma factor in phage cross-resistance. Finally, the infectivity pattern of eleven phages across a panel of 23 genome sequenced strains indicates that additional constraints and interactions beyond the host factors uncovered here define the phage host range.

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2021-12-15
2022-01-28
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References

  1. Breitbart M, Rohwer F. Here a virus, there a virus, everywhere the same virus?. Trends Microbiol 2005; 13:278–284 [View Article] [PubMed]
    [Google Scholar]
  2. Suttle CA. Marine viruses--major players in the global ecosystem. Nat Rev Microbiol 2007; 5:801–812 [View Article] [PubMed]
    [Google Scholar]
  3. Koskella B, Taylor TB. Multifaceted impacts of bacteriophages in the plant microbiome. Annu Rev Phytopathol 2018; 56:361–380 [View Article] [PubMed]
    [Google Scholar]
  4. Shkoporov AN, Hill C. Bacteriophages of the Human Gut: The “Known Unknown” of the Microbiome. Cell Host Microbe 2019; 25:195–209 [View Article] [PubMed]
    [Google Scholar]
  5. Abedon ST. Chapter 1 phage evolution and ecology. In Advances in Applied Microbiology Academic Press; 2009 pp 1–45
    [Google Scholar]
  6. Young R, Gill JJ. Phage therapy redux—What is to be done?. Science 2015; 350:1163–1164 [View Article]
    [Google Scholar]
  7. Rostøl JT, Marraffini L. Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe 2019; 25:184–194 [View Article] [PubMed]
    [Google Scholar]
  8. Samson JE, Magadán AH, Sabri M, Moineau S. Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 2013; 11:675–687 [View Article] [PubMed]
    [Google Scholar]
  9. Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S et al. Phage-bacteria infection networks. Trends Microbiol 2013; 21:82–91 [View Article] [PubMed]
    [Google Scholar]
  10. de Jonge PA, Nobrega FL, Brouns SJJ, Dutilh BE. Molecular and evolutionary determinants of bacteriophage host range. Trends Microbiol 2019; 27:51–63 [View Article] [PubMed]
    [Google Scholar]
  11. Nobrega FL, Vlot M, de Jonge PA, Dreesens LL, Beaumont HJE et al. Targeting mechanisms of tailed bacteriophages. Nat Rev Microbiol 2018; 16:760–773 [View Article] [PubMed]
    [Google Scholar]
  12. Brüssow H. Bacteriophage-host interaction: from splendid isolation into a messy reality. Curr Opin Microbiol 2013; 16:500–506 [View Article] [PubMed]
    [Google Scholar]
  13. De Smet J, Hendrix H, Blasdel BG, Danis-Wlodarczyk K, Lavigne R. Pseudomonas predators: understanding and exploiting phage-host interactions. Nat Rev Microbiol 2017; 15:517–530 [View Article] [PubMed]
    [Google Scholar]
  14. Casjens SR, Hendrix RW. Bacteriophage lambda: Early pioneer and still relevant. Virology 2015; 479–480:310–330 [View Article] [PubMed]
    [Google Scholar]
  15. Calendar R. The Bacteriophages Berlin: Springer Science & Business Media; 2012
    [Google Scholar]
  16. Molineux I. T7 bacteriophages. In Encyclopedia of Molecular Biology New Jersey: John Wiley & Sons, Inc; 2002
    [Google Scholar]
  17. Karam JD, Drake JW. Molecular Biology of Bacteriophage T4 Washington, DC: American Society for Microbiology; 1994
    [Google Scholar]
  18. Díaz-Muñoz SL, Koskella B. Bacteria-phage interactions in natural environments. Adv Appl Microbiol 2014; 89:135–183 [View Article] [PubMed]
    [Google Scholar]
  19. Mirzaei MK, Maurice CF. Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol 2017; 15:397–408 [View Article] [PubMed]
    [Google Scholar]
  20. Lenski RE. Dynamics of interactions between bacteria and virulent bacteriophage. In Marshall KC. eds Advances in Microbial Ecology Boston, MA: Springer US; 1988 pp 1–44
    [Google Scholar]
  21. Campbell A. The future of bacteriophage biology. Nat Rev Genet 2003; 4:471–477 [View Article] [PubMed]
    [Google Scholar]
  22. Keen EC, Adhya SL. Phage therapy: current research and applications. Clin Infect Dis 2015; 61:141–142 [View Article]
    [Google Scholar]
  23. Pirnay J-P, Kutter E. Bacteriophages: it’s a medicine, Jim, but not as we know it. The Lancet Infectious Diseases 2021; 21:309–311 [View Article]
    [Google Scholar]
  24. Gordillo Altamirano FL, Barr JJ. Phage therapy in the postantibiotic era. Clin Microbiol Rev 2019; 32:e00066-18 [View Article] [PubMed]
    [Google Scholar]
  25. Kortright KE, Chan BK, Koff JL, Turner PE. Phage therapy: a renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 2019; 25:219–232 [View Article] [PubMed]
    [Google Scholar]
  26. Chan BK, Sistrom M, Wertz JE, Kortright KE, Narayan D et al. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci Rep 2016; 6:26717 [View Article] [PubMed]
    [Google Scholar]
  27. Gordillo Altamirano F, Forsyth JH, Patwa R, Kostoulias X, Trim M et al. Bacteriophage-resistant Acinetobacter baumannii are resensitized to antimicrobials. Nat Microbiol 2021; 6:157–161 [View Article] [PubMed]
    [Google Scholar]
  28. Wright RCT, Friman V-P, Smith MCM, Brockhurst MA. Cross-resistance is modular in bacteria-phage interactions. PLoS Biol 2018; 16:e2006057–22 [View Article] [PubMed]
    [Google Scholar]
  29. Trudelle DM, Bryan DW, Hudson LK, Denes TG. Cross-resistance to phage infection in Listeria monocytogenes serotype 1/2a mutants. Food Microbiol 2019; 84:103239 [View Article] [PubMed]
    [Google Scholar]
  30. Shin H, Lee J-H, Kim H, Choi Y, Heu S et al. Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica Serovar Typhimurium. PLoS ONE 2012; 7:e43392 [View Article]
    [Google Scholar]
  31. Mangalea MR, Duerkop BA. Fitness trade-offs resulting from bacteriophage resistance potentiate synergistic antibacterial strategies. Infect Immun 2020; 88:e00926-19 [View Article] [PubMed]
    [Google Scholar]
  32. Chan BK, Abedon ST, Loc-Carrillo C. Phage cocktails and the future of phage therapy. Future Microbiol 2013; 8:769–783 [View Article] [PubMed]
    [Google Scholar]
  33. Bai J, Jeon B, Ryu S. Effective inhibition of Salmonella Typhimurium in fresh produce by a phage cocktail targeting multiple host receptors. Food Microbiol 2019; 77:52–60 [View Article] [PubMed]
    [Google Scholar]
  34. Tanji Y, Shimada T, Yoichi M, Miyanaga K, Hori K et al. Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 2004; 64:270–274 [View Article] [PubMed]
    [Google Scholar]
  35. Yen M, Cairns LS, Camilli A. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat Commun 2017; 8:14187 [View Article] [PubMed]
    [Google Scholar]
  36. Hudson HP, Lindberg AA, Stocker BAD. Lipopolysaccharide Core Defects in Salmonella typhimurium Mutants Which Are Resistant to Felix O Phage but Retain Smooth Character. J Gen Microbiol 1978; 109:97–112 [View Article]
    [Google Scholar]
  37. Samuel ADT, Pitta TP, Ryu WS, Danese PN, Leung ECW et al. Flagellar determinants of bacterial sensitivity to chi -phage. Proceedings of the National Academy of Sciences 1999; 96:9863–9866 [View Article]
    [Google Scholar]
  38. Tu J, Park T, Morado DR, Hughes KT, Molineux IJ et al. Dual host specificity of phage SP6 is facilitated by tailspike rotation. Virology 2017; 507:206–215 [View Article] [PubMed]
    [Google Scholar]
  39. Wright A, McConnell M, Kanegasaki S. Lipopolysaccharide as a bacteriophage receptor. In Randall LL, Philipson L. eds Virus Receptors: Part 1 Bacterial Viruses. Springer Netherlands, Dordrecht 1980 pp 27–57
    [Google Scholar]
  40. Lindberg AA, Hellerqvist CG. Bacteriophage attachment sites, serological specificity, and chemical composition of the lipopolysaccharides of semirough and rough mutants of Salmonella typhimurium. J Bacteriol 1971; 105:57–64 [View Article] [PubMed]
    [Google Scholar]
  41. Marti R, Zurfluh K, Hagens S, Pianezzi J, Klumpp J et al. Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC. Mol Microbiol 2013; 87:818–834 [View Article] [PubMed]
    [Google Scholar]
  42. Christen M, Beusch C, Bösch Y, Cerletti D, Flores-Tinoco CE et al. Quantitative selection analysis of bacteriophage φCbK Susceptibility in Caulobacter crescentus. J Mol Biol 2016; 428:419–430 [View Article] [PubMed]
    [Google Scholar]
  43. Chan BK, Turner PE. High-throughput discovery of phage receptors using transposon insertion sequencing of bacteria. PNAS 202018670–18679
    [Google Scholar]
  44. Cowley LA, Low AS, Pickard D, Boinett CJ, Dallman TJ et al. Transposon insertion sequencing elucidates novel gene involvement in susceptibility and resistance to phages T4 and T7 in Escherichia coli O157. mBio 2018; 9:e00705-18 [View Article] [PubMed]
    [Google Scholar]
  45. Pickard D, Kingsley RA, Hale C, Turner K, Sivaraman K et al. A genomewide mutagenesis screen identifies multiple genes contributing to Vi capsular expression in Salmonella enterica serovar Typhi. J Bacteriol 2013; 195:1320–1326 [View Article] [PubMed]
    [Google Scholar]
  46. Bohm K, Porwollik S, Chu W, Dover JA, Gilcrease EB et al. Genes affecting progression of bacteriophage P22 infection in Salmonella identified by transposon and single gene deletion screens. Mol Microbiol 2018; 108:288–305 [View Article] [PubMed]
    [Google Scholar]
  47. Mutalik VK, Adler BA, Rishi HS, Piya D, Zhong C et al. High-throughput mapping of the phage resistance landscape in E. coli. PLoS Biol 2020; 18:e3000877 [View Article]
    [Google Scholar]
  48. Carim S, Azadeh AL, Kazakov AE, Price MN, Walian PJ et al. Systematic Discovery of Pseudomonad Genetic Factors Involved in Sensitivity to Tailocins Cold Spring Harbor Laboratory; 2020
    [Google Scholar]
  49. Mutalik VK, Novichkov PS, Price MN, Owens TK, Callaghan M et al. Dual-barcoded shotgun expression library sequencing for high-throughput characterization of functional traits in bacteria. Nat Commun 2019; 10:308 [View Article] [PubMed]
    [Google Scholar]
  50. Rousset F, Cui L, Siouve E, Becavin C, Depardieu F et al. Genome-wide CRISPR-dCas9 screens in E. coli identify essential genes and phage host factors. PLoS Genet 2018; 14:e1007749 [View Article] [PubMed]
    [Google Scholar]
  51. Wetmore KM, Price MN, Waters RJ, Lamson JS, He J et al. Rapid quantification of mutant fitness in diverse bacteria by sequencing randomly bar-coded transposons. mBio 2015; 6:e00306–15 [View Article]
    [Google Scholar]
  52. Maculloch B, Hoffmann S, Batz M. Economic Burden of Major Foodborne Illnesses Acquired in the United States CreateSpace Independent Publishing Platform; 2015
    [Google Scholar]
  53. Lee J-H, Shin H, Choi Y, Ryu S. Complete genome sequence analysis of bacterial-flagellum-targeting bacteriophage chi. Arch Virol 2013; 158:2179–2183 [View Article] [PubMed]
    [Google Scholar]
  54. Schwartz M. Interaction of phages with their receptor proteins. In Randall LL, Philipson L. eds Virus Receptors: Part 1 Bacterial Viruses Dordrecht: Springer Netherlands; 1980 pp 59–94
    [Google Scholar]
  55. Graña D, Youderian P, Susskind MM. Mutations that improve the ant promoter of Salmonella phage P22. Genetics 1985; 110:1–16 [View Article] [PubMed]
    [Google Scholar]
  56. MacPhee DG, Krishnapillai V, Roantree RJ, Stocker BA. Mutations in Salmonella typhimurium conferring resistance to Felix O phage without loss of smooth character. J Gen Microbiol 1975; 87:1–10 [View Article] [PubMed]
    [Google Scholar]
  57. Wilkinson RG, Gemski P, Stocker BA. Non-smooth mutants of Salmonella typhimurium: differentiation by phage sensitivity and genetic mapping. J Gen Microbiol 1972; 70:527–554 [View Article] [PubMed]
    [Google Scholar]
  58. Islam MS, Zhou Y, Liang L, Nime I, Liu K et al. Application of a phage cocktail for control of Salmonella in foods and reducing biofilms. Viruses 2019; 11:E841 [View Article] [PubMed]
    [Google Scholar]
  59. Gao R, Naushad S, Moineau S, Levesque R, Goodridge L et al. Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica. BMC Genomics 2020; 21:374 [View Article]
    [Google Scholar]
  60. Petsong K, Benjakul S, Chaturongakul S, Switt AIM, Vongkamjan K. Lysis profiles of salmonella phages on salmonella isolates from various sources and efficiency of a phage cocktail against S. Enteritidis and S. Typhimurium. Microorganisms 2019; 7:E100 [View Article] [PubMed]
    [Google Scholar]
  61. Zschach H, Joensen KG, Lindhard B, Lund O, Goderdzishvili M et al. What can we learn from a metagenomic analysis of a georgian bacteriophage cocktail?. Viruses 2015; 7:6570–6589 [View Article] [PubMed]
    [Google Scholar]
  62. McCallin S, Sarker SA, Sultana S, Oechslin F, Brüssow H. Metagenome analysis of Russian and Georgian Pyophage cocktails and a placebo-controlled safety trial of single phage versus phage cocktail in healthy Staphylococcus aureus carriers. Environ Microbiol 2018; 20:3278–3293 [View Article] [PubMed]
    [Google Scholar]
  63. Medalla F, Gu W, Mahon BE, Judd M, Folster J et al. Estimated incidence of antimicrobial drug–resistant nontyphoidal Salmonella infections, United States, 2004–2012. Emerg Infect Dis 2016; 23:29–37 [View Article]
    [Google Scholar]
  64. Centers for Disease Control and Prevention (U.S.) Antibiotic Resistance Threats in the United States; 2019
  65. Kutter E, Sulakvelidze A. Bacteriophages. In Bacteriophages: Biology and Applications CRC Press; 2004 [View Article]
    [Google Scholar]
  66. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: The United States Department of Energy Systems Biology Knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article] [PubMed]
    [Google Scholar]
  67. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  68. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Research in Computational Molecular Biology Berlin Heidelberg: Springer; 2013 pp 158–170
    [Google Scholar]
  69. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article] [PubMed]
    [Google Scholar]
  70. Garneau JR, Depardieu F, Fortier L-C, Bikard D. PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 2017; 7: [View Article]
    [Google Scholar]
  71. Liu H, Price MN, Waters RJ, Ray J, Carlson HK et al. Magic Pools: Parallel Assessment of Transposon Delivery Vectors in Bacteria. mSystems 2018; 3: [View Article]
    [Google Scholar]
  72. Price MN, Wetmore KM, Waters RJ, Callaghan M, Ray J et al. Mutant phenotypes for thousands of bacterial genes of unknown function. Nature 2018; 557:503–509 [View Article] [PubMed]
    [Google Scholar]
  73. Porwollik S, Santiviago CA, Cheng P, Long F, Desai P et al. Defined single-gene and multi-gene deletion mutant collections in Salmonella enterica sv Typhimurium. PLoS One 2014; 9:e99820 [View Article] [PubMed]
    [Google Scholar]
  74. Sawitzke JA, Thomason LC, Costantino N, Bubunenko M, Datta S et al. Recombineering: in vivo genetic engineering in E. coli, S. enterica, and beyond. In Methods in Enzymology Academic Press; 2007 pp 171–199
    [Google Scholar]
  75. Burgin AB, Parodos K, Lane DJ, Pace NR. The excision of intervening sequences from Salmonella 23S ribosomal RNA. Cell 1990; 60:405–414 [View Article] [PubMed]
    [Google Scholar]
  76. Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 2019; 37:907–915 [View Article] [PubMed]
    [Google Scholar]
  77. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 2015; 33:290–295 [View Article] [PubMed]
    [Google Scholar]
  78. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:550 [View Article] [PubMed]
    [Google Scholar]
  79. Beltran P, Plock SA, Smith NH, Whittam TS, Old DC et al. Reference collection of strains of the Salmonella typhimurium complex from natural populations. J Gen Microbiol 1991; 137:601–606 [View Article] [PubMed]
    [Google Scholar]
  80. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  81. Gautreau G, Bazin A, Gachet M, Planel R, Burlot L et al. PPanGGOLiN: Depicting microbial diversity via a partitioned pangenome graph. PLoS Comput Biol 2020; 16:e1007732 [View Article]
    [Google Scholar]
  82. Heinrichs DE, Yethon JA, Whitfield C. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 1998; 30:221–232 [View Article] [PubMed]
    [Google Scholar]
  83. Seif Y, Monk JM, Machado H, Kavvas E, Palsson BO. Systems biology and pangenome of Salmonella O-antigens. mBio 2019; 10:e01247-19 [View Article] [PubMed]
    [Google Scholar]
  84. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  85. Broadbent SE, Davies MR, van der Woude MW. Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Mol Microbiol 2010; 77:337–353 [View Article] [PubMed]
    [Google Scholar]
  86. Roberts RJ, Vincze T, Posfai J, Macelis D. REBASE--a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 2015; 43:D298–9 [View Article] [PubMed]
    [Google Scholar]
  87. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  88. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH, Hancock J. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019 [View Article]
    [Google Scholar]
  89. Katoh K, Standley DM. MAFFT: iterative refinement and additional methods. Methods Mol Biol 2014; 1079:131–146 [View Article] [PubMed]
    [Google Scholar]
  90. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  91. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  92. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
    [Google Scholar]
  93. Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL et al. MUMmer4: A fast and versatile genome alignment system. PLoS Comput Biol 2018; 14:e1005944 [View Article] [PubMed]
    [Google Scholar]
  94. Fu S, Hiley L, Octavia S, Tanaka MM, Sintchenko V et al. Comparative genomics of Australian and international isolates of Salmonella Typhimurium: correlation of core genome evolution with CRISPR and prophage profiles. Sci Rep 2017; 7:9733 [View Article] [PubMed]
    [Google Scholar]
  95. Mariscotti JF, García-del Portillo F. Genome expression analyses revealing the modulation of the Salmonella Rcs regulon by the attenuator IgaA. J Bacteriol 2009; 191:1855–1867 [View Article] [PubMed]
    [Google Scholar]
  96. Cho S-H, Szewczyk J, Pesavento C, Zietek M, Banzhaf M et al. Detecting envelope stress by monitoring β-barrel assembly. Cell 2014; 159:1652–1664 [View Article] [PubMed]
    [Google Scholar]
  97. Gebhart D, Williams SR, Scholl D. Bacteriophage SP6 encodes a second tailspike protein that recognizes Salmonella enterica serogroups C2 and C3. Virology 2017; 507:263–266 [View Article] [PubMed]
    [Google Scholar]
  98. Slauch JM, Lee AA, Mahan MJ, Mekalanos JJ. Molecular characterization of the oafA locus responsible for acetylation of Salmonella typhimurium O-antigen: oafA is a member of a family of integral membrane trans-acylases. J Bacteriol 1996; 178:5904–5909 [View Article] [PubMed]
    [Google Scholar]
  99. Heller K, Braun V. Polymannose o-antigens of Escherichia coli. J Virol 1982; 41:222–227
    [Google Scholar]
  100. Kim M, Ryu S. Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol Microbiol 2012; 86:411–425 [View Article] [PubMed]
    [Google Scholar]
  101. Roantree RJ, Kuo TT, MacPhee DG. The effect of defined lipopolysaccharide core defects upon antibiotic resistances of Salmonella typhimurium. J Gen Microbiol 1977; 103:223–234 [View Article] [PubMed]
    [Google Scholar]
  102. Sanderson KE, MacAlister T, Costerton JW, Cheng KJ. Permeability of lipopolysaccharide-deficient (rough) mutants of Salmonella typhimurium to antibiotics, lysozyme, and other agents. Can J Microbiol 1974; 20:1135–1145 [View Article] [PubMed]
    [Google Scholar]
  103. Wright RCT, Friman V-P, Smith MCM, Brockhurst MA. Resistance evolution against phage combinations depends on the timing and order of exposure. mBio 2019; 10:e01652-19 [View Article] [PubMed]
    [Google Scholar]
  104. Betts A, Gifford DR, MacLean RC, King KC. Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria-phage system. Evolution 2016; 70:969–978 [View Article] [PubMed]
    [Google Scholar]
  105. Hesse S, Rajaure M, Wall E, Johnson J, Bliskovsky V et al. Phage resistance in multidrug-resistant Klebsiella pneumoniae ST258 evolves via diverse mutations that culminate in impaired adsorption. mBio 2020; 11:e02530-19 [View Article] [PubMed]
    [Google Scholar]
  106. Goosen N, van de Putte P. The regulation of transcription initiation by integration host factor. Mol Microbiol 1995; 16:1–7 [View Article] [PubMed]
    [Google Scholar]
  107. Kortright KE, Chan BK, Turner PE. High-throughput discovery of phage receptors using transposon insertion sequencing of bacteria. Proc Natl Acad Sci U S A 2020; 117:18670–18679 [View Article] [PubMed]
    [Google Scholar]
  108. Klose KE, Mekalanos JJ. Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect Immun 1997; 65:587–596 [View Article] [PubMed]
    [Google Scholar]
  109. Su J, Gong H, Lai J, Main A, Lu S. The potassium transporter Trk and external potassium modulate Salmonella enterica protein secretion and virulence. Infect Immun 2009; 77:667–675 [View Article] [PubMed]
    [Google Scholar]
  110. Shariat N, Timme RE, Pettengill JB, Barrangou R, Dudley EG. Characterization and evolution of Salmonella CRISPR-Cas systems. Microbiology 2015; 161:374–386 [View Article]
    [Google Scholar]
  111. Barrangou R, van der Oost J. Bacteriophage exclusion, a new defense system. EMBO J 2015; 34:134–135 [View Article] [PubMed]
    [Google Scholar]
  112. Fang FC, Libby SJ, Buchmeier NA, Loewen PC, Switala J et al. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci U S A 1992; 89:11978–11982 [View Article] [PubMed]
    [Google Scholar]
  113. Chen CY, Buchmeier NA, Libby S, Fang FC, Krause M et al. Central regulatory role for the RpoS sigma factor in expression of Salmonella dublin plasmid virulence genes. J Bacteriol 1995; 177:5303–5309 [View Article] [PubMed]
    [Google Scholar]
  114. Nickerson CA, Curtiss R. Role of sigma factor RpoS in initial stages of Salmonella typhimurium infection. Infect Immun 1997; 65:1814–1823 [View Article] [PubMed]
    [Google Scholar]
  115. Ibanez-Ruiz M, Robbe-Saule V, Hermant D, Labrude S, Norel F. Identification of RpoS (sigma(S))-regulated genes in Salmonella enterica serovar typhimurium. J Bacteriol 2000; 182:5749–5756 [View Article] [PubMed]
    [Google Scholar]
  116. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 2002; 66:373–395 [View Article] [PubMed]
    [Google Scholar]
  117. Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 2011; 65:189–213 [View Article] [PubMed]
    [Google Scholar]
  118. Lévi-Meyrueis C, Monteil V, Sismeiro O, Dillies M-A, Monot M et al. Expanding the RpoS/σS-network by RNA sequencing and identification of σS-controlled small RNAs in Salmonella. PLoS One 2014; 9:e96918–12 [View Article] [PubMed]
    [Google Scholar]
  119. Lago M, Monteil V, Douche T, Guglielmini J, Criscuolo A et al. Proteome remodelling by the stress sigma factor RpoS/σS in Salmonella: identification of small proteins and evidence for post-transcriptional regulation. Sci Rep 2017; 7:2127 [View Article] [PubMed]
    [Google Scholar]
  120. Lucchini S, McDermott P, Thompson A, Hinton JCD. The H-NS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium. Mol Microbiol 2009; 74:1169–1186 [View Article] [PubMed]
    [Google Scholar]
  121. Wilmes-Riesenberg MR, Foster JW, Curtiss R. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun 1997; 65:203–210 [View Article] [PubMed]
    [Google Scholar]
  122. Samuels DJ, Frye JG, Porwollik S, McClelland M, Mrázek J et al. Use of a promiscuous, constitutively-active bacterial enhancer-binding protein to define the σ54 (RpoN) regulon of Salmonella Typhimurium LT2. BMC Genomics 2013; 14:602 [View Article] [PubMed]
    [Google Scholar]
  123. Aurass P, Düvel J, Karste S, Nübel U, Rabsch W et al. glnA Truncation in Salmonella enterica results in a small colony variant phenotype, attenuated host cell entry, and reduced expression of flagellin and SPI-1-Associated Effector Genes. Appl Environ Microbiol 2018; 84:3687 [View Article]
    [Google Scholar]
  124. Hyman P, Abedon ST. Chapter 7 - bacteriophage host range and bacterial resistance. In Advances in Applied Microbiology Academic Press; 2010 pp 217–248
    [Google Scholar]
  125. Holmfeldt K, Middelboe M, Nybroe O, Riemann L. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl Environ Microbiol 2007; 73:6730–6739 [View Article] [PubMed]
    [Google Scholar]
  126. Moller AG, Lindsay JA, Read TD. Determinants of phage host range in Staphylococcus species. Appl Environ Microbiol 2019; 85:e00209-19 [View Article] [PubMed]
    [Google Scholar]
  127. Rabsch W. Salmonella typhimurium phage typing for pathogens. Methods Mol Biol 2007; 394:177–211 [View Article] [PubMed]
    [Google Scholar]
  128. Chirakadze I, Perets A, Ahmed R. Phage typing. Methods Mol Biol 2009; 502:293–305 [View Article] [PubMed]
    [Google Scholar]
  129. Canals R, Hammarlöf DL, Kröger C, Owen SV, Fong WY et al. Adding function to the genome of African Salmonella Typhimurium ST313 strain D23580. PLoS Biol 2019; 17:e3000059 [View Article] [PubMed]
    [Google Scholar]
  130. Richardson EJ, Limaye B, Inamdar H, Datta A, Manjari KS et al. Genome sequences of Salmonella enterica serovar typhimurium, Choleraesuis, Dublin, and Gallinarum strains of well- defined virulence in food-producing animals. J Bacteriol 2011; 193:3162–3163 [View Article] [PubMed]
    [Google Scholar]
  131. Fu S, Octavia S, Tanaka MM, Sintchenko V, Lan R. Defining the Core Genome of Salmonella enterica Serovar Typhimurium for Genomic Surveillance and Epidemiological Typing. J Clin Microbiol 2015; 53:2530–2538 [View Article] [PubMed]
    [Google Scholar]
  132. Hoare A, Bittner M, Carter J, Alvarez S, Zaldívar M et al. The outer core lipopolysaccharide of Salmonella enterica serovar Typhi is required for bacterial entry into epithelial cells. Infect Immun 2006; 74:1555–1564 [View Article] [PubMed]
    [Google Scholar]
  133. Washizaki A, Yonesaki T, Otsuka Y. Characterization of the interactions between Escherichia coli receptors, LPS and OmpC, and bacteriophage T4 long tail fibers. Microbiologyopen 2016; 5:1003–1015 [View Article] [PubMed]
    [Google Scholar]
  134. Davies MR, Broadbent SE, Harris SR, Thomson NR, van der Woude MW. Horizontally acquired glycosyltransferase operons drive salmonellae lipopolysaccharide diversity. PLoS Genet 2013; 9:e1003568 [View Article] [PubMed]
    [Google Scholar]
  135. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS et al. Prophages mediate defense against phage infection through diverse mechanisms. ISME J 2016; 10:2854–2866 [View Article] [PubMed]
    [Google Scholar]
  136. Wahl A, Battesti A, Ansaldi M. Prophages in Salmonella enterica: a driving force in reshaping the genome and physiology of their bacterial host?. Mol Microbiol 2019; 111:303–316 [View Article] [PubMed]
    [Google Scholar]
  137. Owen SV, Wenner N, Dulberger CL, Rodwell EV. Prophage-encoded phage defence proteins with cognate self-immunity. bioRxiv 2020
    [Google Scholar]
  138. Vasu K, Nagaraja V. Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 2013; 77:53–72 [View Article] [PubMed]
    [Google Scholar]
  139. Cota I, Sánchez-Romero MA, Hernández SB, Pucciarelli MG, García-Del Portillo F et al. Epigenetic Control of Salmonella enterica O-Antigen Chain Length: A Tradeoff between Virulence and Bacteriophage Resistance. PLoS Genet 2015; 11:e1005667 [View Article] [PubMed]
    [Google Scholar]
  140. Dedrick RM, Jacobs-Sera D, Bustamante CAG, Garlena RA, Mavrich TN et al. Prophage-mediated defence against viral attack and viral counter-defence. Nat Microbiol 2017; 2:16251 [View Article] [PubMed]
    [Google Scholar]
  141. Bernheim A, Sorek R. The pan-immune system of bacteria: antiviral defence as a community resource. Nat Rev Microbiol 2020; 18:113–119 [View Article] [PubMed]
    [Google Scholar]
  142. Dy RL, Richter C, Salmond GPC, Fineran PC. Remarkable Mechanisms in Microbes to Resist Phage Infections. Annu Rev Virol 2014; 1:307–331 [View Article] [PubMed]
    [Google Scholar]
  143. van Houte S, Buckling A, Westra ER. Evolutionary Ecology of Prokaryotic Immune Mechanisms. Microbiol Mol Biol Rev 2016; 80:745–763 [View Article] [PubMed]
    [Google Scholar]
  144. Nagy G, Danino V, Dobrindt U, Pallen M, Chaudhuri R et al. Down-regulation of key virulence factors makes the Salmonella enterica serovar Typhimurium rfaH mutant a promising live-attenuated vaccine candidate. Infect Immun 2006; 74:5914–5925 [View Article] [PubMed]
    [Google Scholar]
  145. Toguchi A, Siano M, Burkart M, Harshey RM. Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J Bacteriol 2000; 182:6308–6321 [View Article] [PubMed]
    [Google Scholar]
  146. Kong Q, Yang J, Liu Q, Alamuri P, Roland KL et al. Effect of deletion of genes involved in lipopolysaccharide core and O-antigen synthesis on virulence and immunogenicity of Salmonella enterica serovar typhimurium. Infect Immun 2011; 79:4227–4239 [View Article] [PubMed]
    [Google Scholar]
  147. Robbe-Saule V, Coynault C, Norel F. The live oral typhoid vaccine Ty21a is a rpoS mutant and is susceptible to various environmental stresses. FEMS Microbiol Lett 1995; 126:171–176 [View Article] [PubMed]
    [Google Scholar]
  148. Battesti A, Majdalani N, Gottesman S. Stress sigma factor RpoS degradation and translation are sensitive to the state of central metabolism. Proc Natl Acad Sci U S A 2015; 112:5159–5164 [View Article] [PubMed]
    [Google Scholar]
  149. Dong T, Schellhorn HE. Role of RpoS in virulence of pathogens. Infect Immun 2010; 78:887–897 [View Article] [PubMed]
    [Google Scholar]
  150. Crawford RW, Keestra AM, Winter SE, Xavier MN, Tsolis RM et al. Very long O-antigen chains enhance fitness during Salmonella-induced colitis by increasing bile resistance. PLoS Pathog 2012; 8:e1002918 [View Article] [PubMed]
    [Google Scholar]
  151. Domínguez-Medina CC, Pérez-Toledo M, Schager AE, Marshall JL, Cook CN et al. Outer membrane protein size and LPS O-antigen define protective antibody targeting to the Salmonella surface. Nat Commun 2020; 11:851 [View Article] [PubMed]
    [Google Scholar]
  152. Brandão A, Pires DP, Coppens L, Voet M, Lavigne R et al. Differential transcription profiling of the phage LUZ19 infection process in different growth media. RNA Biology 2021; 18:1778–1790 [View Article]
    [Google Scholar]
  153. Howard-Varona C, Hargreaves KR, Solonenko NE, Markillie LM, White RA et al. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME J 2018; 12:1605–1618 [View Article] [PubMed]
    [Google Scholar]
  154. Rishi HS, Toro E, Liu H, Wang X, LS Q et al. Systematic genome-wide querying of coding and non-coding functional elements in e. coli using crispri. bioRxiv 2020
    [Google Scholar]
  155. Thibault D, Jensen PA, Wood S, Qabar C, Clark S et al. Droplet Tn-Seq combines microfluidics with Tn-Seq for identifying complex single-cell phenotypes. Nat Commun 2019; 10:5729 [View Article] [PubMed]
    [Google Scholar]
  156. Chan BK, Turner PE, Kim S, Mojibian HR, Elefteriades JA et al. Phage treatment of an aortic graft infected with Pseudomonas aeruginosa. Evol Med Public Health 2018; 2018:60–66 [View Article] [PubMed]
    [Google Scholar]
  157. Schade SZ, Adler J, Ris H. How bacteriophage chi attacks motile bacteria. J Virol 1967; 1:599–609 [View Article] [PubMed]
    [Google Scholar]
  158. Steinbacher S, Miller S, Baxa U, Budisa N, Weintraub A et al. Phage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 A, fully refined structure of the endorhamnosidase at 1.56 A resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 1997; 267:865–880 [View Article] [PubMed]
    [Google Scholar]
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