1887

Abstract

is an opportunistic food-borne bacterium that is capable of infecting humans with high rates of hospitalization and mortality. Natural populations are genotypically and phenotypically variable, with some lineages being responsible for most human infections. The success of is linked to its capacity to persist on food and in the environment. Biofilms are an important feature that allow these bacteria to persist and infect humans, so understanding the genetic basis of biofilm formation is key to understanding transmission. We sought to investigate the biofilm-forming ability of by identifying genetic variation that underlies biofilm formation in natural populations using genome-wide association studies (GWAS). Changes in gene expression of specific strains during biofilm formation were then investigated using RNA sequencing (RNA-seq). Genetic variation associated with enhanced biofilm formation was identified in 273 genes by GWAS and differential expression in 220 genes by RNA-seq. Statistical analyses show that the number of overlapping genes flagged by either type of experiment is less than expected by random sampling. This novel finding is consistent with an evolutionary scenario where rapid adaptation is driven by variation in gene expression of pioneer genes, and this is followed by slower adaptation driven by nucleotide changes within the core genome.

Funding
This study was supported by the:
  • Medical Research Council (Award MR/L015080/1)
    • Principle Award Recipient: SamuelK Sheppard
  • Medical Research Council (Award MR/S009264/1)
    • Principle Award Recipient: SamuelK Sheppard
  • Medical Research Council (Award MR/V001213/1)
    • Principle Award Recipient: SamuelK Sheppard
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001114
2023-10-18
2024-07-20
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/10/mgen001114.html?itemId=/content/journal/mgen/10.1099/mgen.0.001114&mimeType=html&fmt=ahah

References

  1. Farber JM, Peterkin PI. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 1991; 55:476–511 [View Article] [PubMed]
    [Google Scholar]
  2. Murray EGD, Webb RA, Swann MBR. A disease of rabbits characterised by a large mononuclear leucocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes (n.sp.). J Pathol 1926; 29:407–439 [View Article]
    [Google Scholar]
  3. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS et al. Food-related illness and death in the United States. Emerg Infect Dis 1999; 5:607–625 [View Article] [PubMed]
    [Google Scholar]
  4. Pizarro-Cerdá J, Cossart P. Microbe profile: Listeria monocytogenes: a paradigm among intracellular bacterial pathogens. Microbiology 2019; 165:719–721 [View Article] [PubMed]
    [Google Scholar]
  5. European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2017. EFS2 2018; 16:e05500 [View Article]
    [Google Scholar]
  6. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 2011; 17:7–15 [View Article]
    [Google Scholar]
  7. Grønstøl H. Listeriosis in sheep. Acta Vet Scand 1980; 21:11–17 [View Article]
    [Google Scholar]
  8. Hellström S, Kiviniemi K, Autio T, Korkeala H. Listeria monocytogenes is common in wild birds in Helsinki region and genotypes are frequently similar with those found along the food chain. J Appl Microbiol 2008; 104:883–888 [View Article] [PubMed]
    [Google Scholar]
  9. Mpundu P, Muma JB, Mukumbuta N, Mukubesa AN, Muleya W et al. Isolation, discrimination, and molecular detection of Listeria species from slaughtered cattle in Namwala District, Zambia. BMC Microbiol 2022; 22:160 [View Article] [PubMed]
    [Google Scholar]
  10. Rothrock MJ, Davis ML, Locatelli A, Bodie A, McIntosh TG et al. Listeria occurrence in poultry flocks: detection and potential implications. Front Vet Sci 2017; 4:125 [View Article]
    [Google Scholar]
  11. Kayode AJ, Okoh AI. Assessment of multidrug-resistant Listeria monocytogenes in milk and milk product and one health perspective. PLoS One 2022; 17:e0270993 [View Article] [PubMed]
    [Google Scholar]
  12. Osman KM, Kappell AD, Fox EM, Orabi A, Samir A. Prevalence, pathogenicity, virulence, antibiotic resistance, and phylogenetic analysis of biofilm-producing Listeria monocytogenes isolated from different ecological niches in Egypt: food, humans, animals, and environment. Pathogens 2020; 9:5 [View Article] [PubMed]
    [Google Scholar]
  13. Osman KM, Zolnikov TR, Samir A, Orabi A. Prevalence, pathogenic capability, virulence genes, biofilm formation, and antibiotic resistance of Listeria in goat and sheep milk confirms need of hygienic milking conditions. Pathog Glob Health 2014; 108:21–29 [View Article] [PubMed]
    [Google Scholar]
  14. Linke K, Rückerl I, Brugger K, Karpiskova R, Walland J et al. Reservoirs of Listeria species in three environmental ecosystems. Appl Environ Microbiol 2014; 80:5583–5592 [View Article] [PubMed]
    [Google Scholar]
  15. Mpondo L, Ebomah KE, Okoh AI. Multidrug-resistant Listeria species shows abundance in environmental waters of a key district municipality in South Africa. Int J Environ Res Public Health 2021; 18:481 [View Article] [PubMed]
    [Google Scholar]
  16. Ramaswamy V, Cresence VM, Rejitha JS, Lekshmi MU, Dharsana KS et al. Listeria--review of epidemiology and pathogenesis. J Microbiol Immunol Infect 2007; 40:4–13 [PubMed]
    [Google Scholar]
  17. Vivant AL, Garmyn D, Gal L, Hartmann A, Piveteau P. Survival of Listeria monocytogenes in soil requires AgrA-mediated regulation. Appl Environ Microbiol 2015; 81:5073–5084 [View Article] [PubMed]
    [Google Scholar]
  18. Zhu Q, Gooneratne R, Hussain MA. Listeria monocytogenes in fresh produce: outbreaks, prevalence and contamination levels. Foods 2017; 6:21 [View Article] [PubMed]
    [Google Scholar]
  19. Werbrouck H, Grijspeerdt K, Botteldoorn N, Van Pamel E, Rijpens N et al. Differential inlA and inlB expression and interaction with human intestinal and liver cells by Listeria monocytogenes strains of different origins. Appl Environ Microbiol 2006; 72:3862–3871 [View Article] [PubMed]
    [Google Scholar]
  20. Dalton CB, Austin CC, Sobel J, Hayes PS, Bibb WF et al. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med 1997; 336:100–105 [View Article] [PubMed]
    [Google Scholar]
  21. Longhi C, Conte MP, Penta M, Cossu A, Antonini G et al. Lactoferricin influences early events of Listeria monocytogenes infection in THP-1 human macrophages. J Med Microbiol 2004; 53:87–91 [View Article] [PubMed]
    [Google Scholar]
  22. Orsi RH, den Bakker HC, Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 2011; 301:79–96 [View Article] [PubMed]
    [Google Scholar]
  23. Moura A, Lefrancq N, Wirth T, Leclercq A, Borges V et al. Emergence and global spread of Listeria monocytogenes main clinical clonal complex. Sci Adv 2021; 7:eabj9805 [View Article] [PubMed]
    [Google Scholar]
  24. Nightingale KK, Ivy RA, Ho AJ, Fortes ED, Njaa BL et al. inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Appl Environ Microbiol 2008; 74:6570–6583 [View Article] [PubMed]
    [Google Scholar]
  25. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008; 4:e1000146 [View Article] [PubMed]
    [Google Scholar]
  26. Bergholz TM, Shah MK, Burall LS, Rakic-Martinez M, Datta AR. Genomic and phenotypic diversity of Listeria monocytogenes clonal complexes associated with human listeriosis. Appl Microbiol Biotechnol 2018; 102:3475–3485 [View Article] [PubMed]
    [Google Scholar]
  27. Palumbo JD, Borucki MK, Mandrell RE, Gorski L. Serotyping of Listeria monocytogenes by enzyme-linked immunosorbent assay and identification of mixed-serotype cultures by colony immunoblotting. J Clin Microbiol 2003; 41:564–571 [View Article] [PubMed]
    [Google Scholar]
  28. Gasanov U, Hughes D, Hansbro PM. Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol Rev 2005; 29:851–875 [View Article] [PubMed]
    [Google Scholar]
  29. Lee S, Ward TJ, Graves LM, Tarr CL, Siletzky RM et al. Population structure of Listeria monocytogenes serotype 4b isolates from sporadic human listeriosis cases in the United States from 2003 to 2008. Appl Environ Microbiol 2014; 80:3632–3644 [View Article] [PubMed]
    [Google Scholar]
  30. Swaminathan B, Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect 2007; 9:1236–1243 [View Article] [PubMed]
    [Google Scholar]
  31. López D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harb Perspect Biol 2010; 2:a000398 [View Article] [PubMed]
    [Google Scholar]
  32. Otto M. Physical stress and bacterial colonization. FEMS Microbiol Rev 2014; 38:1250–1270 [View Article] [PubMed]
    [Google Scholar]
  33. Lee BH, Hébraud M, Bernardi T. Increased adhesion of Listeria monocytogenes strains to abiotic surfaces under cold stress. Front Microbiol 2017; 8:2221 [View Article] [PubMed]
    [Google Scholar]
  34. Møretrø T, Langsrud S. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms 2004; 1:107–121 [View Article]
    [Google Scholar]
  35. Greenwood MH, Roberts D, Burden P. The occurrence of Listeria species in milk and dairy products: a national survey in England and Wales. Int J Food Microbiol 1991; 12:197–206 [View Article] [PubMed]
    [Google Scholar]
  36. Rodríguez-Campos D, Rodríguez-Melcón C, Alonso-Calleja C, Capita R. Persistent Listeria monocytogenes isolates from a poultry-processing facility form more biofilm but do not have a greater resistance to disinfectants than sporadic strains. Pathogens 2019; 8:250 [View Article] [PubMed]
    [Google Scholar]
  37. Sofos JN, Geornaras I. Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157:H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci 2010; 86:2–14 [View Article] [PubMed]
    [Google Scholar]
  38. Ulusoy BH, Chirkena K. Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the antibiotic resistance. Food Quality and Safety 2019; 3:233–241 [View Article]
    [Google Scholar]
  39. Becker LA, Evans SN, Hutkins RW, Benson AK. Role of sigma(B) in adaptation of Listeria monocytogenes to growth at low temperature. J Bacteriol 2000; 182:7083–7087 [View Article] [PubMed]
    [Google Scholar]
  40. Bucur FI, Grigore-Gurgu L, Crauwels P, Riedel CU, Nicolau AI. Resistance of Listeria monocytogenes to stress conditions encountered in food and food processing environments. Front Microbiol 2018; 9:2700 [View Article] [PubMed]
    [Google Scholar]
  41. Chan YC, Wiedmann M. Physiology and genetics of Listeria monocytogenes survival and growth at cold temperatures. Crit Rev Food Sci Nutr 2009; 49:237–253 [View Article] [PubMed]
    [Google Scholar]
  42. Conficoni D, Losasso C, Cortini E, Di Cesare A, Cibin V et al. Resistance to biocides in Listeria monocytogenes collected in meat-processing environments. Front Microbiol 2016; 7:1627 [View Article]
    [Google Scholar]
  43. Skowron K, Wałecka-Zacharska E, Grudlewska K, Gajewski P, Wiktorczyk N et al. Disinfectant susceptibility of biofilm formed by Listeria monocytogenes under selected environmental conditions. Microorganisms 2019; 7:280 [View Article]
    [Google Scholar]
  44. Wiktorczyk-Kapischke N, Skowron K, Grudlewska-Buda K, Wałecka-Zacharska E, Korkus J et al. Adaptive response of Listeria monocytogenes to the stress factors in the food processing environment. Front Microbiol 2021; 12:710085 [View Article] [PubMed]
    [Google Scholar]
  45. Wiśniewski P, Zakrzewski AJ, Zadernowska A, Chajęcka-Wierzchowska W. Antimicrobial resistance and virulence characterization of Listeria monocytogenes strains isolated from food and food processing environments. Pathogens 2022; 11:1099 [View Article] [PubMed]
    [Google Scholar]
  46. McLauchlin J, Grant KA, Amar CFL. Human foodborne listeriosis in England and Wales, 1981 to 2015. Epidemiol Infect 2020; 148:e54 [View Article] [PubMed]
    [Google Scholar]
  47. Meldrum RJ, Little CL, Sagoo S, Mithani V, McLauchlin J et al. Assessment of the microbiological safety of salad vegetables and sauces from kebab take-away restaurants in the United Kingdom. Food Microbiol 2009; 26:573–577 [View Article] [PubMed]
    [Google Scholar]
  48. Colagiorgi A, Di Ciccio P, Zanardi E, Ghidini S, Ianieri A. A look inside the Listeria monocytogenes biofilms extracellular matrix. Microorganisms 2016; 4:22 [View Article] [PubMed]
    [Google Scholar]
  49. Lemon KP, Higgins DE, Kolter R. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 2007; 189:4418–4424 [View Article] [PubMed]
    [Google Scholar]
  50. Popowska M, Krawczyk-Balska A, Ostrowski R, Desvaux M. InlL from Listeria monocytogenes is involved in biofilm formation and adhesion to mucin. Front Microbiol 2017; 8:660 [View Article]
    [Google Scholar]
  51. Aidley J, Wanford JJ, Green LR, Sheppard SK, Bayliss CD. PhasomeIt: an “omics” approach to cataloguing the potential breadth of phase variation in the genus Campylobacter. Microb Genom 2018; 4:e000228 [View Article] [PubMed]
    [Google Scholar]
  52. Brooks JL, Jefferson KK. Phase variation of poly-N-acetylglucosamine expression in Staphylococcus aureus. PLoS Pathog 2014; 10:e1004292 [View Article] [PubMed]
    [Google Scholar]
  53. Levinson G, Gutman GA. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 1987; 4:203–221 [View Article] [PubMed]
    [Google Scholar]
  54. Manuel CS, Van Stelten A, Wiedmann M, Nightingale KK, Orsi RH. Prevalence and distribution of Listeria monocytogenes inlA alleles prone to phase variation and inlA alleles with premature stop codon mutations among human, food, animal, and environmental isolates. Appl Environ Microbiol 2015; 81:8339–8345 [View Article] [PubMed]
    [Google Scholar]
  55. den Bakker HC, Didelot X, Fortes ED, Nightingale K, Wiedmann M. Lineage specific recombination rates and microevolution in Listeria monocytogenes. BMC Evol Biol 2008; 8:277 [View Article] [PubMed]
    [Google Scholar]
  56. Corvin A, Craddock N, Sullivan PF. Genome-wide association studies: a primer. Psychol Med 2010; 40:1063–1077 [View Article]
    [Google Scholar]
  57. Sheppard SK, Didelot X, Meric G, Torralbo A, Jolley KA et al. Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci U S A 2013; 110:11923–11927 [View Article] [PubMed]
    [Google Scholar]
  58. Uffelmann E, Huang QQ, Munung NS, de Vries J, Okada Y et al. Genome-wide association studies. Nat Rev Methods Primers 2021; 1:59 [View Article]
    [Google Scholar]
  59. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article] [PubMed]
    [Google Scholar]
  60. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2016; 2:16185 [View Article] [PubMed]
    [Google Scholar]
  61. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article] [PubMed]
    [Google Scholar]
  62. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  63. Mack D, Nedelmann M, Krokotsch A, Schwarzkopf A, Heesemann J et al. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 1994; 62:3244–3253 [View Article] [PubMed]
    [Google Scholar]
  64. Pascoe B, Méric G, Murray S, Yahara K, Mageiros L et al. Enhanced biofilm formation and multi-host transmission evolve from divergent genetic backgrounds in Campylobacter jejuni. Environ Microbiol 2015; 17:4779–4789 [View Article] [PubMed]
    [Google Scholar]
  65. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  66. Bayliss SC, Thorpe HA, Coyle NM, Sheppard SK, Feil EJ. PIRATE: a fast and scalable pangenomics toolbox for clustering diverged orthologues in bacteria. Gigascience 2019; 8:giz119 [View Article] [PubMed]
    [Google Scholar]
  67. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  68. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLOS Comput Biol 2015; 11:e1004041 [View Article] [PubMed]
    [Google Scholar]
  69. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 2017; 14:417–419 [View Article] [PubMed]
    [Google Scholar]
  70. Huber W, Carey VJ, Gentleman R, Anders S, Carlson M et al. Orchestrating high-throughput genomic analysis with bioconductor. Nat Methods 2015; 12:115–121 [View Article] [PubMed]
    [Google Scholar]
  71. 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]
  72. Lees JA, Galardini M, Bentley SD, Weiser JN, Corander J. pyseer: a comprehensive tool for microbial pangenome-wide association studies. Bioinformatics 2018; 34:4310–4312 [View Article] [PubMed]
    [Google Scholar]
  73. Lees JA, Mai TT, Galardini M, Wheeler NE, Horsfield ST et al. Improved prediction of bacterial genotype-phenotype associations using interpretable pangenome-spanning regressions. mBio 2020; 11:e01344-20 [View Article] [PubMed]
    [Google Scholar]
  74. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:Genomics 2013
    [Google Scholar]
  75. Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res 2023; 51:D587–D592 [View Article] [PubMed]
    [Google Scholar]
  76. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016; 44:D457–62 [View Article] [PubMed]
    [Google Scholar]
  77. Bucher T, Oppenheimer-Shaanan Y, Savidor A, Bloom-Ackermann Z, Kolodkin-Gal I. Disturbance of the bacterial cell wall specifically interferes with biofilm formation. Environ Microbiol Rep 2015; 7:990–1004 [View Article] [PubMed]
    [Google Scholar]
  78. Iwashkiw JA, Seper A, Weber BS, Scott NE, Vinogradov E et al. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog 2012; 8:e1002758 [View Article] [PubMed]
    [Google Scholar]
  79. Greenwich J, Reverdy A, Gozzi K, Di Cecco G, Tashjian T et al. A decrease in serine levels during growth transition triggers biofilm formation in Bacillus subtilis. J Bacteriol 2019; 201:e00155-19 [View Article] [PubMed]
    [Google Scholar]
  80. Harmsen M, Lappann M, Knøchel S, Molin S. Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 2010; 76:2271–2279 [View Article] [PubMed]
    [Google Scholar]
  81. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R et al. D-amino acids trigger biofilm disassembly. Science 2010; 328:627–629 [View Article] [PubMed]
    [Google Scholar]
  82. Lu H, Que Y, Wu X, Guan T, Guo H. Metabolomics deciphered metabolic reprogramming required for biofilm formation. Sci Rep 2019; 9:13160 [View Article]
    [Google Scholar]
  83. Liu R, Gao D, Fang Z, Zhao L, Xu Z et al. AroC, a chorismate synthase, is required for the formation of Edwardsiella tarda biofilms. Microbes Infect 2022; 24:104955 [View Article] [PubMed]
    [Google Scholar]
  84. Puttamreddy S, Cornick NA, Minion FC. Genome-wide transposon mutagenesis reveals a role for pO157 genes in biofilm development in Escherichia coli O157:H7 EDL933. Infect Immun 2010; 78:2377–2384 [View Article] [PubMed]
    [Google Scholar]
  85. Shemesh M, Tam A, Steinberg D. Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology 2007; 153:1307–1317 [View Article] [PubMed]
    [Google Scholar]
  86. Santos T, Viala D, Chambon C, Esbelin J, Hébraud M. Listeria monocytogenes biofilm adaptation to different temperatures seen through shotgun proteomics. Front Nutr 2019; 6:89 [View Article]
    [Google Scholar]
  87. Ryan S, Begley M, Gahan CGM, Hill C. Molecular characterization of the arginine deiminase system in Listeria monocytogenes: regulation and role in acid tolerance. Environ Microbiol 2009; 11:432–445 [View Article] [PubMed]
    [Google Scholar]
  88. Jakubovics NS, Robinson JC, Samarian DS, Kolderman E, Yassin SA et al. Critical roles of arginine in growth and biofilm development by Streptococcus gordonii. Mol Microbiol 2015; 97:281–300 [View Article] [PubMed]
    [Google Scholar]
  89. Robinson JC, Rostami N, Casement J, Vollmer W, Rickard AH et al. ArcR modulates biofilm formation in the dental plaque colonizer Streptococcus gordonii. Mol Oral Microbiol 2018; 33:143–154 [View Article] [PubMed]
    [Google Scholar]
  90. Melian C, Castellano P, Segli F, Mendoza LM, Vignolo GM. Proteomic analysis of Listeria monocytogenes FBUNT during biofilm formation at 10°C in response to lactocin AL705. Front Microbiol 2021; 12:604126 [View Article] [PubMed]
    [Google Scholar]
  91. Zhang H-P, Kang Y-H, Kong L-C, Ju A-Q, Wang Y-M et al. Functional analysis of hisJ in Aeromonas veronii reveals a key role in virulence. Ann N Y Acad Sci 2020; 1465:146–160 [View Article] [PubMed]
    [Google Scholar]
  92. Ge X, Kitten T, Chen Z, Lee SP, Munro CL et al. Identification of Streptococcus sanguinis genes required for biofilm formation and examination of their role in endocarditis virulence. Infect Immun 2008; 76:2551–2559 [View Article] [PubMed]
    [Google Scholar]
  93. Assisi C, Forauer E, Oliver HF, Etter AJ. Genomic and transcriptomic analysis of biofilm formation in persistent and transient Listeria monocytogenes isolates from the retail deli environment does not yield insight into persistence mechanisms. Foodborne Pathog Dis 2021; 18:179–188 [View Article] [PubMed]
    [Google Scholar]
  94. Travier L, Guadagnini S, Gouin E, Dufour A, Chenal-Francisque V et al. ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. PLoS Pathog 2013; 9:e1003131 [View Article] [PubMed]
    [Google Scholar]
  95. Alonso AN, Perry KJ, Regeimbal JM, Regan PM, Higgins DE. Identification of Listeria monocytogenes determinants required for biofilm formation. PLoS One 2014; 9:e113696 [View Article] [PubMed]
    [Google Scholar]
  96. Janež N, Škrlj B, Sterniša M, Klančnik A, Sabotič J. The role of the Listeria monocytogenes surfactome in biofilm formation. Microb Biotechnol 2021; 14:1269–1281 [View Article] [PubMed]
    [Google Scholar]
  97. Nakao R, Ramstedt M, Wai SN, Uhlin BE. Enhanced biofilm formation by Escherichia coli LPS mutants defective in hep biosynthesis. PLoS One 2012; 7:e51241 [View Article] [PubMed]
    [Google Scholar]
  98. Nakao R, Senpuku H, Watanabe H. Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect Immun 2006; 74:6145–6153 [View Article] [PubMed]
    [Google Scholar]
  99. Wu C, Al Mamun AAM, Luong TT, Hu B, Gu J et al. Forward genetic dissection of biofilm development by Fusobacterium nucleatum: novel functions of cell division proteins FtsX and EnvC. mBio 2018; 9:e00360-18 [View Article] [PubMed]
    [Google Scholar]
  100. Li Q, Li Z, Li X, Xia L, Zhou X et al. FtsEX-CwlO regulates biofilm formation by a plant-beneficial rhizobacterium Bacillus velezensis SQR9. Res Microbiol 2018; 169:166–176 [View Article] [PubMed]
    [Google Scholar]
  101. Osek J, Lachtara B, Wieczorek K. Listeria monocytogenes - How this pathogen survives in food-production environments?. Front Microbiol 2022; 13:866462 [View Article] [PubMed]
    [Google Scholar]
  102. Hutchins C, Sayavedra L, Diaz M, Gupta P, Tissingh E et al. Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials. Sci Rep 2021; 11:21864 [View Article] [PubMed]
    [Google Scholar]
  103. van Teeffelen S, Gitai Z. Rotate into shape: MreB and bacterial morphogenesis. EMBO J 2011; 30:4856–4857 [View Article] [PubMed]
    [Google Scholar]
  104. Stülke J, Krüger L. Cyclic di-AMP signaling in bacteria. Annu Rev Microbiol 2020; 74:159–179 [View Article] [PubMed]
    [Google Scholar]
  105. Peng X, Zhang Y, Bai G, Zhou X, Wu H. Cyclic di-AMP mediates biofilm formation. Mol Microbiol 2016; 99:945–959 [View Article] [PubMed]
    [Google Scholar]
  106. Wang M, Wamp S, Gibhardt J, Holland G, Schwedt I et al. Adaptation of Listeria monocytogenes to perturbation of c-di-AMP metabolism underpins its role in osmoadaptation and identifies a fosfomycin uptake system. Environ Microbiol 2022; 24:4466–4488 [View Article] [PubMed]
    [Google Scholar]
  107. Whiteley AT, Garelis NE, Peterson BN, Choi PH, Tong L et al. c-di-AMP modulates Listeria monocytogenes central metabolism to regulate growth, antibiotic resistance and osmoregulation. Mol Microbiol 2017; 104:212–233 [View Article] [PubMed]
    [Google Scholar]
  108. Devaraj A, Buzzo JR, Mashburn-Warren L, Gloag ES, Novotny LA et al. The extracellular DNA lattice of bacterial biofilms is structurally related to holliday junction recombination intermediates. Proc Natl Acad Sci U S A 2019; 116:25068–25077 [View Article] [PubMed]
    [Google Scholar]
  109. Iwasaki H, Takahagi M, Nakata A, Shinagawa H. Escherichia coli RuvA and RuvB proteins specifically interact with holliday junctions and promote branch migration. Genes Dev 1992; 6:2214–2220 [View Article] [PubMed]
    [Google Scholar]
  110. Du H, Pang M, Dong Y, Wu Y, Wang N et al. Identification and characterization of an Aeromonas hydrophila oligopeptidase gene pepF negatively related to biofilm formation. Front Microbiol 2016; 7:1497 [View Article] [PubMed]
    [Google Scholar]
  111. Sela S, Frank S, Belausov E, Pinto R. A Mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol 2006; 72:5653–5658 [View Article] [PubMed]
    [Google Scholar]
  112. Niu C, Robbins CM, Pittman KJ, Osborn joDi L, Stubblefield BA et al. LuxS influences Escherichia coli biofilm formation through autoinducer-2-dependent and autoinducer-2-independent modalities. FEMS Microbiol Ecol 2013; 83:778–791 [View Article] [PubMed]
    [Google Scholar]
  113. Merritt J, Qi F, Goodman SD, Anderson MH, Shi W. Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 2003; 71:1972–1979 [View Article] [PubMed]
    [Google Scholar]
  114. Cole SP, Harwood J, Lee R, She R, Guiney DG. Characterization of monospecies biofilm formation by Helicobacter pylori. J Bacteriol 2004; 186:3124–3132 [View Article] [PubMed]
    [Google Scholar]
  115. Di Bonaventura G, Piccolomini R, Paludi D, D’Orio V, Vergara A et al. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J Appl Microbiol 2008; 104:1552–1561 [View Article] [PubMed]
    [Google Scholar]
  116. Govaert M, Smet C, Baka M, Janssens T, Impe JV. Influence of incubation conditions on the formation of model biofilms by Listeria monocytogenes and Salmonella Typhimurium on abiotic surfaces. J Appl Microbiol 2018; 125: [View Article] [PubMed]
    [Google Scholar]
  117. Gründling A, Burrack LS, Bouwer HGA, Higgins DE. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc Natl Acad Sci U S A 2004; 101:12318–12323 [View Article] [PubMed]
    [Google Scholar]
  118. Kobras CM, Fenton AK, Sheppard SK. Next-generation microbiology: from comparative genomics to gene function. Genome Biol 2021; 22:123 [View Article] [PubMed]
    [Google Scholar]
  119. Sheppard SK, Guttman DS, Fitzgerald JR. Population genomics of bacterial host adaptation. Nat Rev Genet 2018; 19:549–565 [View Article] [PubMed]
    [Google Scholar]
  120. Lebreton A, Cossart P. RNA- and protein-mediated control of Listeria monocytogenes virulence gene expression. RNA Biol 2017; 14:460–470 [View Article] [PubMed]
    [Google Scholar]
  121. Casadesús J, Low D. Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 2006; 70:830–856 [View Article] [PubMed]
    [Google Scholar]
  122. Manuel CS, Van Stelten A, Wiedmann M, Nightingale KK, Orsi RH. Prevalence and distribution of Listeria monocytogenes inlA alleles prone to phase variation and inlA alleles with premature stop codon mutations among human, food, animal, and environmental isolates. Appl Environ Microbiol 2015; 81:8339–8345 [View Article] [PubMed]
    [Google Scholar]
  123. Bervoets I, Charlier D. Diversity, versatility and complexity of bacterial gene regulation mechanisms: opportunities and drawbacks for applications in synthetic biology. FEMS Microbiol Rev 2019; 43:304–339 [View Article] [PubMed]
    [Google Scholar]
  124. Brockman KL, Azzari PN, Branstool MT, Atack JM, Schulz BL et al. Epigenetic regulation alters biofilm architecture and composition in multiple clinical isolates of nontypeable haemophilus influenzae. mBio 2018; 9:e01682-18 [View Article] [PubMed]
    [Google Scholar]
  125. Chia N, Woese CR, Goldenfeld N. A collective mechanism for phase variation in biofilms. Proc Natl Acad Sci U S A 2008; 105:14597–14602 [View Article] [PubMed]
    [Google Scholar]
  126. Harris LG, Murray S, Pascoe B, Bray J, Meric G et al. Biofilm morphotypes and population structure among Staphylococcus epidermidis from commensal and clinical samples. PLoS One 2016; 11:e0151240 [View Article] [PubMed]
    [Google Scholar]
  127. He X, Ahn J. Differential gene expression in planktonic and biofilm cells of multiple antibiotic-resistant SalmonellaTyphimurium and Staphylococcus aureus. FEMS Microbiol Lett 2011; 325:180–188 [View Article]
    [Google Scholar]
  128. Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol 2003; 48:253–267 [View Article]
    [Google Scholar]
  129. Toliopoulos C, Giaouris E. Marked inter-strain heterogeneity in the differential expression of some key stress response and virulence-related genes between planktonic and biofilm cells in Listeria monocytogenes. Int J Food Microbiol 2023; 390:110136 [View Article] [PubMed]
    [Google Scholar]
  130. Händel N, Schuurmans JM, Feng Y, Brul S, ter Kuile BH. Interaction between mutations and regulation of gene expression during development of de novo antibiotic resistance. Antimicrob Agents Chemother 2014; 58:4371–4379 [View Article] [PubMed]
    [Google Scholar]
  131. Serra DO, Hengge R. Stress responses go three dimensional - the spatial order of physiological differentiation in bacterial macrocolony biofilms. Environ Microbiol 2014; 16:1455–1471 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001114
Loading
/content/journal/mgen/10.1099/mgen.0.001114
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL

Supplementary material 4

EXCEL

Supplementary material 5

EXCEL

Supplementary material 6

EXCEL

Supplementary material 7

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error