1932

Abstract

Bacteria are social organisms that commonly live in dense communities surrounded by a multitude of other species. The competitive and cooperative interactions between these species not only shape the bacterial communities but also influence their susceptibility to antimicrobials. While several studies have shown that mixed-species communities are more tolerant toward antimicrobials than their monospecies counterparts, only limited empirical data are currently available on how interspecies interactions influence resistance development. We here propose a theoretic framework outlining the potential impact of interspecies social behavior on different aspects of resistance development. We identify factors by which interspecies interactions might influence resistance evolution and distinguish between their effect on () the emergence of a resistant mutant and () the spread of this resistance throughout the population. Our analysis indicates that considering the social life of bacteria is imperative to the rational design of more effective antibiotic treatment strategies with a minimal hazard for resistance development.

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2022-09-08
2024-06-13
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Literature Cited

  1. 1.
    Adamowicz EM, Flynn J, Hunter RC, Harcombe WR. 2018. Cross-feeding modulates antibiotic tolerance in bacterial communities. ISME J 12:112723–35
    [Google Scholar]
  2. 2.
    Adamowicz EM, Muza M, Chacón JM, Harcombe WR. 2020. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLOS Pathog 16:7e1008700
    [Google Scholar]
  3. 3.
    Amanatidou E, Matthews AC, Kuhlicke U, Neu TR, McEvoy JP, Raymond B 2019. Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli. npj Biofilms Microbiomes 5:136
    [Google Scholar]
  4. 4.
    Andersson DI, Hughes D. 2014. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 12:7465–78
    [Google Scholar]
  5. 5.
    Barbosa C, Roemhild R, Rosenstiel P, Schulenburg H. 2019. Evolutionary stability of collateral sensitivity to antibiotics in the model pathogen Pseudomonas aeruginosa. eLife 8:e51481
    [Google Scholar]
  6. 6.
    Baümler AJ, Sperandio V. 2016. Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535:761085–93
    [Google Scholar]
  7. 7.
    Beaber JW, Hochhut B, Waldor MK. 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:696972–74
    [Google Scholar]
  8. 8.
    Borgeaud S, Metzger LC, Scrignari T, Blokesch M. 2015. The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 347:621763–67
    [Google Scholar]
  9. 9.
    Bottery MJ, Matthews JL, Wood AJ, Krogh Johansen H, Pitchford JW, Friman V-P 2022. Inter-species interactions alter antibiotic efficacy in bacterial communities. ISME J. 16:3812–21
    [Google Scholar]
  10. 10.
    Bottery MJ, Pitchford JW, Friman VP. 2021. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J 15:4939–48
    [Google Scholar]
  11. 11.
    Brauner A, Fridman O, Gefen O, Balaban NQ. 2016. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat. Rev. Microbiol. 14:5320–30
    [Google Scholar]
  12. 12.
    Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ. 2014. Interactions in multispecies biofilms: Do they actually matter?. Trends Microbiol 22:284–91
    [Google Scholar]
  13. 13.
    Carlson SA, Frana TS, Griffith RW. 2001. Antibiotic resistance in Salmonella enterica serovar Typhimurium exposed to microcin-producing Escherichia coli. Society 67:83763–66
    [Google Scholar]
  14. 14.
    Cianfanelli FR, Monlezun L, Coulthurst SJ. 2016. Aim, load, fire: the type VI secretion system, a bacterial nanoweapon. Trends Microbiol 24:151–62
    [Google Scholar]
  15. 15.
    Cohen NR, Lobritz MA, Collins JJ. 2013. Microbial persistence and the road to drug resistance. Cell Host Microbe 13:6632–42
    [Google Scholar]
  16. 16.
    Colijn C, Cohen T. 2015. How competition governs whether moderate or aggressive treatment minimizes antibiotic resistance. eLife 4:e10559
    [Google Scholar]
  17. 17.
    Connell JL, Ritschdorff ET, Whiteley M, Shear JB. 2013. 3D printing of microscopic bacterial communities. PNAS 110:4618380–85
    [Google Scholar]
  18. 18.
    Cornforth DM, Foster KR. 2013. Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol. 11:4285–93
    [Google Scholar]
  19. 19.
    Dickey SW, Cheung GYC, Otto M. 2017. Different drugs for bad bugs: antivirulence strategies in the age of antibiotic resistance. Nat. Rev. Drug Discov. 16:7457–71
    [Google Scholar]
  20. 20.
    D'Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C 2018. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat. Prod. Rep. 35:5455–88
    [Google Scholar]
  21. 21.
    Dugatkin LA, Perlin M, Lucas JS, Atlas R. 2005. Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm. Proc. R. Soc. B 272:155879–83
    [Google Scholar]
  22. 22.
    Estrela S, Brown SP. 2018. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLOS Comput. Biol. 14:6e1006179
    [Google Scholar]
  23. 23.
    Fair RJ, Tor Y. 2014. Antibiotics and bacterial resistance in the 21st century. Perspect. Medicin. Chem. 6:25–64
    [Google Scholar]
  24. 24.
    Fierer N, Lennon JT. 2011. The generation and maintenance of diversity in microbial communities. Am. J. Bot. 98:3439–48
    [Google Scholar]
  25. 25.
    Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S 2016. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14:9563–75
    [Google Scholar]
  26. 26.
    Foster KR, Bell T. 2012. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22:191845–50
    [Google Scholar]
  27. 27.
    Frapwell CJ, Howlin RP, Soren O, McDonagh BT, Duignan CM et al. 2018. Increased rates of genomic mutation in a biofilm co-culture model of Pseudomonas aeruginosa and Staphylococcus aureus. bioRxiv 387233, Aug. 21 (Preprint)
  28. 28.
    Fridman O, Goldberg A, Ronin I, Shoresh N, Balaban NQ. 2014. Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations. Nature 513:7518418–21
    [Google Scholar]
  29. 29.
    Frost I, Smith WPJ, Mitri S, Millan AS, Davit Y et al. 2018. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J 12:61582–93
    [Google Scholar]
  30. 30.
    Fusco D, Gralka M, Kayser J, Anderson A, Hallatschek O 2016. Excess of mutational jackpot events in expanding populations revealed by spatial Luria-Delbrück experiments. Nat. Commun. 7:12760
    [Google Scholar]
  31. 31.
    Galhardo RS, Hastings PJ, Rosenberg SM. 2007. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42:5399–435
    [Google Scholar]
  32. 32.
    Gjødsbøl K, Christensen JJ, Karlsmark T, Jørgensen B, Klein BM, Krogfelt KA. 2006. Multiple bacterial species reside in chronic wounds: a longitudinal study. Int. Wound J. 3:3225–31
    [Google Scholar]
  33. 33.
    Gómez P, Buckling A. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:6025106–9
    [Google Scholar]
  34. 34.
    Goneau LW, Yeoh NS, MacDonald KW, Cadieux PA, Burton JP et al. 2014. Selective target inactivation rather than global metabolic dormancy causes antibiotic tolerance in uropathogens. Antimicrob. Agents Chemother. 58:42089–97
    [Google Scholar]
  35. 35.
    Hibbing ME, Fuqua C, Parsek MR, Peterson SB. 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8:115–25
    [Google Scholar]
  36. 36.
    Howden BP, Davies JK, Johnson PDR, Stinear TP, Grayson ML. 2010. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancoycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin. Microbiol. Rev. 23:199–139
    [Google Scholar]
  37. 37.
    Huddleston JR. 2014. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect. Drug Resist. 7:167–76
    [Google Scholar]
  38. 38.
    Hughes D, Andersson DI. 2012. Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr. Opin. Microbiol. 15:5555–60
    [Google Scholar]
  39. 39.
    Imamovic L, Sommer MOA. 2013. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl. Med. 5:204201ra132
    [Google Scholar]
  40. 40.
    Johnson PJT, Levin BR. 2013. Pharmacodynamics, population dynamics, and the evolution of persistence in Staphylococcus aureus. PLOS Genet 9:1e1003123
    [Google Scholar]
  41. 41.
    Kimura M, Maruyama T, Crow JF. 1963. The mutation load in small populations. Genetics 48:9181303–12
    [Google Scholar]
  42. 42.
    Klümper U, Recker M, Zhang L, Yin X, Zhang T et al. 2019. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J 13:122927–37
    [Google Scholar]
  43. 43.
    Koch G, Yepes A, Förstner KU, Wermser C, Stengel ST et al. 2014. Evolution of resistance to a last-resort antibiotic in Staphylococcus aureus via bacterial competition. Cell 158:51060–71
    [Google Scholar]
  44. 44.
    Kvich L, Burmølle M, Bjarnsholt T, Lichtenberg M. 2020. Do mixed-species biofilms dominate in chronic infections? Need for in situ visualization of bacterial organization. Front. Cell. Infect. Microbiol. 10:396
    [Google Scholar]
  45. 45.
    Layton JC, Foster PL. 2005. Error-prone DNA polymerase IV is regulated by the heat shock chaperone GroE in Escherichia coli. J. Bacteriol. 187:2449–57
    [Google Scholar]
  46. 46.
    Lerminiaux NA, Cameron ADS. 2019. Horizontal transfer of antibiotic resistance genes in clinical environments. Can. J. Microbiol. 65:134–44
    [Google Scholar]
  47. 47.
    Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ. 2017. Antibiotic tolerance facilitates the evolution of resistance. Science 355:6327826–30
    [Google Scholar]
  48. 48.
    Lories B, Roberfroid S, Dieltjens L, De Coster D, Foster KR, Steenackers HP. 2020. Biofilm bacteria use stress responses to detect and respond to competitors. Curr. Biol. 30:71231–44.e4
    [Google Scholar]
  49. 49.
    Maharjan RP, Ferenci T. 2018. The impact of growth rate and environmental factors on mutation rates and spectra in Escherichia coli. Environ. Microbiol. Rep. 10:6626–33
    [Google Scholar]
  50. 50.
    Martínez JL. 2008. Antibiotics and antibiotic resistance genes in natural environments. Science 321:5887365–67
    [Google Scholar]
  51. 51.
    Mathur H, Field D, Rea MC, Cotter PD, Hill C, Ross RP. 2017. Bacteriocin-antimicrobial synergy: a medical and food perspective. Front. Microbiol. 8:1205
    [Google Scholar]
  52. 52.
    Matthey N, Stutzmann S, Stoudmann C, Guex N, Iseli C, Blokesch M. 2019. Neighbor predation linked to natural competence fosters the transfer of large genomic regions in Vibrio cholerae. eLife 8:e48212
    [Google Scholar]
  53. 53.
    McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J et al. 2017. Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat. Commun. 8:14371
    [Google Scholar]
  54. 54.
    Melnyk AH, McCloskey N, Hinz AJ, Dettman J, Kassen R. 2017. Evolution of cost-free resistance under fluctuating drug selection in Pseudomonas aeruginosa. mSphere 2:4e00158–17
    [Google Scholar]
  55. 55.
    Melnyk AH, Wong A, Kassen R. 2015. The fitness costs of antibiotic resistance mutations. Evol. Appl. 8:3273–83
    [Google Scholar]
  56. 56.
    Mitri S, Foster KR. 2013. The genotypic view of social interactions in microbial communities. Annu. Rev. Genet. 47:247–73
    [Google Scholar]
  57. 57.
    Mitri S, Xavier JB, Foster KR. 2011. Social evolution in multispecies biofilms. PNAS 108:Suppl. 210839–46
    [Google Scholar]
  58. 58.
    Montassier E, Valdés-Mas R, Batard E, Zmora N, Dori-Bachash M et al. 2021. Probiotics impact the antibiotic resistance gene reservoir along the human GI tract in a person-specific and antibiotic-dependent manner. Nat. Microbiol. 6:1043–54
    [Google Scholar]
  59. 59.
    Moyano AJ, Luján AM, Argaraña CE, Smania AM. 2007. MutS deficiency and activity of the error-prone DNA polymerase IV are crucial for determining mucA as the main target for mucoid conversion in Pseudomonas aeruginosa. Mol. Microbiol. 64:2547–59
    [Google Scholar]
  60. 60.
    Nadell CD, Drescher K, Foster KR. 2016. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14:9589–600
    [Google Scholar]
  61. 61.
    Nicoloff HH, Andersson DI. 2016. Indirect resistance to several classes of antibiotics in cocultures with resistant bacteria expressing antibiotic-modifying or -degrading enzymes. J. Antimicrob. Chemother. 71:1100–10
    [Google Scholar]
  62. 62.
    Nothias LF, Knight R, Dorrestein PC. 2016. Antibiotic discovery is a walk in the park. PNAS 113:5114477–79
    [Google Scholar]
  63. 63.
    Oz T, Guvenek A, Yildiz S, Karaboga E, Tamer YT et al. 2014. Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution. Mol. Biol. Evol. 31:92387–401
    [Google Scholar]
  64. 64.
    Parijs I, Steenackers HP. 2018. Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms. ISME J 12:82061–75
    [Google Scholar]
  65. 65.
    Perlin MH, Clark DR, Mckenzie C, Patel H, Kormanik C et al. 2009. Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations. Proc. Biol. Sci. 276:16743759–68
    [Google Scholar]
  66. 66.
    Principi N, Silvestri E, Esposito S. 2019. Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front. Pharmacol. 10:513
    [Google Scholar]
  67. 67.
    Que YA, Hazan R, Strobel B, Maura D, He J et al. 2013. A quorum sensing small volatile molecule promotes antibiotic tolerance in bacteria. PLOS ONE 8:12e80140
    [Google Scholar]
  68. 68.
    Riley MA, Gordon DM. 1999. The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7:3129–33
    [Google Scholar]
  69. 69.
    Sharma A, Wood KB. 2021. Spatial segregation and cooperation in radially expanding microbial colonies under antibiotic stress. ISME J. 15:103019
    [Google Scholar]
  70. 70.
    Silva DR, Sardi JCO, Pitangui NS, Roque SM, da Silva ACB, Rosalen PL. 2020. Probiotics as an alternative antimicrobial therapy: current reality and future directions. J. Funct. Foods 73:104080
    [Google Scholar]
  71. 71.
    Sommer F, Bäckhed F. 2013. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 11:4227–38
    [Google Scholar]
  72. 72.
    Song T, Park Y, Shamputa IC, Seo S, Lee SY et al. 2014. Fitness costs of rifampicin-resistance in Mycobacterium tuberculosis are amplified under conditions of nutrient starvation and compensated by mutation in the β′ subunit of RNA polymerase. Mol. Microbiol. 91:61106–19
    [Google Scholar]
  73. 73.
    Sorg RA, Lin L, van Doorn GS, Sorg M, Olson J et al. 2016. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLOS Biol 14:12e2000631
    [Google Scholar]
  74. 74.
    Soucy SM, Huang J, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:8472–82
    [Google Scholar]
  75. 75.
    Steenackers HP, Parijs I, Foster KR, Vanderleyden J. 2016. Experimental evolution in biofilm populations. FEMS Microbiol. Rev. 40:3373–97
    [Google Scholar]
  76. 76.
    Stewart PS. 2015. Antimicrobial tolerance in biofilms. Microbiol. Spectr. 3:3 https://doi.org/10.1128/microbiolspec.MB-0010-2014
    [Crossref] [Google Scholar]
  77. 77.
    Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6:3199–210
    [Google Scholar]
  78. 78.
    Suzuki S, Horinouchi T, Furusawa C. 2017. Acceleration and suppression of resistance development by antibiotic combinations. BMC Genomics 18:1328
    [Google Scholar]
  79. 79.
    Toprak E, Veres A, Michel JB, Chait R, Hartl DL, Kishony R. 2012. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat. Genet. 44:1101–5
    [Google Scholar]
  80. 80.
    Trejo-Hernández A, Andrade-Domínguez A, Hernández M, Encarnación S. 2014. Interspecies competition triggers virulence and mutability in Candida albicansPseudomonas aeruginosa mixed biofilms. ISME J 8:101974–88
    [Google Scholar]
  81. 81.
    Walker D, Rolfe M, Thompson A, Moore GR, James R et al. 2004. Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. J. Bacteriol. 186:3866–69
    [Google Scholar]
  82. 82.
    Wargo AR, Huijben S, De Roode JC, Shepherd J, Read AF. 2007. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. PNAS 104:5019914–19
    [Google Scholar]
  83. 83.
    Welp AL, Bomberger JM. 2020. Bacterial community interactions during chronic respiratory disease. Front. Cell. Infect. Microbiol. 10:213
    [Google Scholar]
  84. 84.
    West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:8597–607
    [Google Scholar]
  85. 85.
    Willi Y, Van Buskirk J, Hoffmann AA. 2006. Limits to the adaptive potential of small populations. Annu. Rev. Ecol. Evol. Syst. 37:433–58
    [Google Scholar]
  86. 86.
    Windels EM, Michiels JE, Fauvart M, Wenseleers T, Van den Bergh B, Michiels J. 2019. Bacterial persistence promotes the evolution of antibiotic resistance by increasing survival and mutation rates. ISME J 13:51239–51
    [Google Scholar]
  87. 87.
    Wistrand-Yuen E, Knopp M, Hjort K, Koskiniemi S, Berg OG, Andersson DI. 2018. Evolution of high-level resistance during low-level antibiotic exposure. Nat. Commun. 9:11599
    [Google Scholar]
  88. 88.
    Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. PNAS 104:3876–81
    [Google Scholar]
  89. 89.
    Yan J, Bassler BL. 2019. Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe 26:115–21
    [Google Scholar]
  90. 90.
    Yurtsev EA, Chao HX, Datta MS, Artemova T, Gore J. 2013. Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol. Syst. Biol. 9:683
    [Google Scholar]
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