1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Microbiology
  4. Volume 71, 2017
  5. Article

Annual Review of Microbiology

Volume 71, 2017

Predator Versus Pathogen: How Does Predatory Interface with the Challenges of Killing Gram-Negative Pathogens in a Host Setting?

Abstract

is a small deltaproteobacterial predator that has evolved to invade, reseal, kill, and digest other gram-negative bacteria in soils and water environments. It has a broad host range and kills many antibiotic-resistant, clinical pathogens in vitro, a potentially useful capability if it could be translated to a clinical setting. We review relevant mechanisms of predation and the physiological properties that would influence its survival in a mammalian host. Bacterial pathogens increasingly display conventional antibiotic resistance by expressing and varying surface and soluble biomolecules. Predators coevolved alongside prey bacteria and so encode diverse predatory enzymes that are hard for pathogens to resist by simple mutation. Predators do not replicate outside pathogens and thus express few transport proteins and thus few surface epitopes for host immune recognition. We explain these features, relating them to the potential of predatory bacteria as cellular medicines.

Keyword(s): antimicrobial resistance, bacterial predators, living antibiotics, predation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090816-093618
2017-09-08
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/71/1/annurev-micro-090816-093618.html?itemId=/content/journals/10.1146/annurev-micro-090816-093618&mimeType=html&fmt=ahah

Literature Cited

  1. Abram D, Castro e Melo J, Chou D. 1.  1974. Penetration of Bdellovibrio bacteriovorus into host cells. J. Bacteriol. 118:663–80 [Google Scholar]
  2. Alexander M. 2.  1981. Why microbial predators and parasites do not eliminate their prey and hosts. Annu. Rev. Microbiol. 35:113–33 [Google Scholar]
  3. Atterbury RJ, Hobley L, Till R, Lambert C, Capeness MJ. 3.  et al. 2011. Effects of orally administered Bdellovibrio bacteriovorus on the well-being and Salmonella colonization of young chicks. Appl. Environ. Microbiol. 77:5794–803 [Google Scholar]
  4. Avidan O, Petrenko M, Becker R, Beck S, Linscheid M. 4.  et al. 2017. Identification and characterization of differentially-regulated type IVb pilin genes necessary for predation in obligate bacterial predators. Sci. Rep. 7:1013 [Google Scholar]
  5. Bjarnsholt T. 5.  2013. The role of bacterial biofilms in chronic infections. APMIS Suppl1361–51 [Google Scholar]
  6. Boll JM, Crofts AA, Peters K, Cattoir V, Vollmer W. 6.  et al. 2016. A penicillin-binding protein inhibits selection of colistin-resistant, lipooligosaccharide-deficient Acinetobacter baumannii. PNAS 113:41E6228–37 [Google Scholar]
  7. Boll JM, Tucker AT, Klein DR, Beltran AM, Brodbelt JS. 7.  et al. 2015. Reinforcing lipid A acylation on the cell surface of Acinetobacter baumannii promotes cationic antimicrobial peptide resistance and desiccation survival. mBio 6:3e00478–15 [Google Scholar]
  8. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D. 8.  et al. 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48:1–12 [Google Scholar]
  9. Capeness MJ, Lambert C, Lovering AL, Till R, Uchida K. 9.  et al. 2013. Activity of Bdellovibrio hit locus proteins, Bd0108 and Bd0109, links type IVa pilus extrusion/retraction status to prey-independent growth signalling. PLOS ONE 8:e79759 [Google Scholar]
  10. Crowley PH, Straley SC, Craig RJ, Culin JD, Fu YT. 10.  et al. 1980. A model of prey bacteria, predator bacteria, and bacteriophage in continuous culture. J. Theor. Biol. 86:377–400 [Google Scholar]
  11. Dashiff A, Junka RA, Libera M, Kadouri DE. 11.  2011. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus. Bdellovibrio bacteriovorus. J. Appl. Microbiol. 110:431–44 [Google Scholar]
  12. Dashiff A, Keeling TG, Kadouri DE. 12.  2011. Inhibition of predation by Bdellovibrio bacteriovorus and Micavibrio aeruginosavorus via host cell metabolic activity in the presence of carbohydrates. Appl. Environ. Microbiol. 77:2224–31 [Google Scholar]
  13. Dattner I, Miller E, Petrenko M, Kadouri DE, Jurkevitch E, Huppert A. 13.  2017. Modelling and parameter inference of predator–prey dynamics in heterogeneous environments using the direct integral approach. J. R. Soc. Interface 14:20160525 [Google Scholar]
  14. Elemam A, Rahimian J, Mandell W. 14.  2009. Infection with panresistant Klebsiella pneumoniae: a report of 2 cases and a brief review of the literature. Clin. Infect. Dis. 49:271–74 [Google Scholar]
  15. Evans KJ, Lambert C, Sockett RE. 15.  2007. Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J. Bacteriol. 189:4850–59 [Google Scholar]
  16. Freire MP, Pierrotti LC, Filho HH, Ibrahim KY, Magri AS. 16.  et al. 2015. Infection with Klebsiella pneumoniae carbapenemase (KPC)-producing Klebsiella pneumoniae in cancer patients. Eur. J. Clin. Microbiol. Infect. Dis. 34:277–86 [Google Scholar]
  17. Gupta S, Tang C, Tran M, Kadouri DE. 17.  2016. Effect of predatory bacteria on human cell lines. PLOS ONE 11:e0161242 [Google Scholar]
  18. Hobley L, King JR, Sockett RE. 18.  2006. Bdellovibrio predation in the presence of decoys: three-way bacterial interactions revealed by mathematical and experimental analyses. Appl. Environ. Microbiol. 72:6757–65 [Google Scholar]
  19. Hobley L, Lerner TR, Williams LE, Lambert C, Till R. 19.  et al. 2012. Genome analysis of a simultaneously predatory and prey-independent, novel Bdellovibrio bacteriovorus from the River Tiber, supports in silico predictions of both ancient and recent lateral gene transfer from diverse bacteria. BMC Genom 13:670 [Google Scholar]
  20. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA. 20.  et al. 2015. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. PNAS 112:E3574–81 [Google Scholar]
  21. Jashnsaz H, Al Juboori M, Weistuch C, Miller N, Nguyen T. 21.  et al. 2017. Hydrodynamic hunters. Biophys. J. 112:1282–89 [Google Scholar]
  22. Kadouri D, O'Toole GA. 22.  2005. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl. Environ. Microbiol. 71:4044–51 [Google Scholar]
  23. Kadouri DE, To K, Shanks RM, Doi Y. 23.  2013. Predatory bacteria: a potential ally against multidrug-resistant gram-negative pathogens. PLOS ONE 8:e63397 [Google Scholar]
  24. Karunker I, Rotem O, Dori-Bachash M, Jurkevitch E, Sorek R. 24.  2013. A global transcriptional switch between the attack and growth forms of Bdellovibrio bacteriovorus. PLOS ONE 8:e61850 [Google Scholar]
  25. Kidd TJ, Mills G, Sá-Pessoa J, Dumigan A, Frank CG. 25.  et al. 2017. A Klebsiella pneumoniae antibiotic resistance mechanism that subdues host defences and promotes virulence. EMBO Mol. Med. 9:430–47 [Google Scholar]
  26. Koval SF, Bayer ME. 26.  1997. Bacterial capsules: no barrier against Bdellovibrio. Microbiology 143:Pt. 3749–53 [Google Scholar]
  27. Koval SF, Hynes SH. 27.  1991. Effect of paracrystalline protein surface layers on predation by Bdellovibrio bacteriovorus. J. Bacteriol. 173:2244–49 [Google Scholar]
  28. Lambert C, Cadby IT, Till R, Bui NK, Lerner TR. 28.  et al. 2015. Ankyrin-mediated self-protection during cell invasion by the bacterial predator Bdellovibrio bacteriovorus. Nat. Commun. 6:8884 [Google Scholar]
  29. Lambert C, Chang CY, Capeness MJ, Sockett RE. 29.  2010. The first bite—profiling the predatosome in the bacterial pathogen Bdellovibrio. PLOS ONE 5:e8599 [Google Scholar]
  30. Lambert C, Evans KJ, Till R, Hobley L, Capeness M. 30.  et al. 2006. Characterizing the flagellar filament and the role of motility in bacterial prey-penetration by Bdellovibrio bacteriovorus. Mol. Microbiol. 60:274–86 [Google Scholar]
  31. Lambert C, Fenton AK, Hobley L, Sockett RE. 31.  2011. Predatory Bdellovibrio bacteria use gliding motility to scout for prey on surfaces. J. Bacteriol. 193:3139–41 [Google Scholar]
  32. Lambert C, Ivanov P, Sockett L. 32.  2010. A transcriptional “scream” early response of E. coli prey to predatory invasion by Bdellovibrio. Curr. Microbiol. 60:419–27 [Google Scholar]
  33. Lambert C, Smith MCM, Sockett RE. 33.  2003. A novel assay to monitor predator-prey interactions for Bdellovibrio bacteriovorus 109J reveals a role for methyl-accepting chemotaxis proteins in predation. Environ. Microbiol. 5:127–32 [Google Scholar]
  34. Lenz RW, Hespell RB. 34.  1978. Attempts to grow bdellovibrios micurgically-injected into animal cells. Arch. Microbiol. 119:245–48 [Google Scholar]
  35. Lerner TR, Lovering AL, Bui NK, Uchida K, Aizawa S. 35.  et al. 2012. Specialized peptidoglycan hydrolases sculpt the intra-bacterial niche of predatory Bdellovibrio and increase population fitness. PLOS Pathog 8:e1002524 [Google Scholar]
  36. Liu B, Knirel YA, Feng L, Perepelov AV, Senchenkova SN. 36.  2014. Structural diversity in Salmonella O antigens and its genetic basis. FEMS Microbiol. Rev. 38:56–89 [Google Scholar]
  37. Livermore DM. 37.  2011. Discovery research: the scientific challenge of finding new antibiotics. J. Antimicrob. Chemother. 66:1941–44 [Google Scholar]
  38. Luciano J, Agrebi R, Le Gall AV, Wartel M, Fiegna F. 38.  et al. 2011. Emergence and modular evolution of a novel motility machinery in bacteria. PLOS Genet 7:e1002268 [Google Scholar]
  39. Mahmoud KK, Koval SF. 39.  2010. Characterization of type IV pili in the life cycle of the predator bacterium Bdellovibrio. Microbiology 156:1040–51 [Google Scholar]
  40. Marchand A, Gabignon O. 40.  1981. Modèle théorique de la cinétique d'interaction du couple proie-prédateur Bdellovibrio bacteriovorus–Escherichia coli [Theoretical model of the predator-prey interaction kinetics between Bdellovibrio bacteriovorus and Escherichia coli].. Ann. Microbiol. 132B:321–36 [Google Scholar]
  41. Medina AA, Shanks RM, Kadouri DE. 41.  2008. Development of a novel system for isolating genes involved in predator-prey interactions using host independent derivatives of Bdellovibrio bacteriovorus 109J. BMC Microbiol 8:33 [Google Scholar]
  42. Mehrad B, Clark NM, Zhanel GG, 3rd Lynch JP. 42.  2015. Antimicrobial resistance in hospital-acquired gram-negative bacterial infections. Chest 147:1413–21 [Google Scholar]
  43. Milner DS, Till R, Cadby I, Lovering AL, Basford SM. 43.  et al. 2014. Ras GTPase-like protein MglA, a controller of bacterial social-motility in myxobacteria, has evolved to control bacterial predation by Bdellovibrio. PLOS Genet. 10:e1004253 [Google Scholar]
  44. Monnappa AK, Bari W, Choi SY, Mitchell RJ. 44.  2016. Investigating the responses of human epithelial cells to predatory bacteria. Sci. Rep. 6:33485 [Google Scholar]
  45. Mostowy S, Boucontet L, Mazon Moya MJ, Sirianni A, Boudinot P. 45.  et al. 2013. The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy. PLOS Pathog 9:e1003588 [Google Scholar]
  46. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL. 46.  et al. 2013. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect. Dis. 13:785–96 [Google Scholar]
  47. Nakamura M. 47.  1972. Alteration of Shigella pathogenicity by other bacteria. Am. J. Clin. Nutr. 25:1441–51 [Google Scholar]
  48. Nordmann P, Cuzon G, Naas T. 48.  2009. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect. Dis. 9:228–36 [Google Scholar]
  49. Pendleton JN, Gorman SP, Gilmore BF. 49.  2013. Clinical relevance of the ESKAPE pathogens. Expert Rev. Anti-Infect. Ther. 11:297–308 [Google Scholar]
  50. Podschun R, Ullmann U. 50.  1998. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 11:589–603 [Google Scholar]
  51. Prehna G, Ramirez BE, Lovering AL. 51.  2014. The lifestyle switch protein Bd0108 of Bdellovibrio bacteriovorus is an intrinsically disordered protein. PLOS ONE 9:e115390 [Google Scholar]
  52. Rice LB. 52.  2008. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J. Infect. Dis. 197:1079–81 [Google Scholar]
  53. Romanowski EG, Stella NA, Brothers KM, Yates KA, Funderburgh ML. 53.  et al. 2016. Predatory bacteria are nontoxic to the rabbit ocular surface. Sci. Rep. 6:30987 [Google Scholar]
  54. Roschanski N, Klages S, Reinhardt R, Linscheid M, Strauch E. 54.  2011. Identification of genes essential for prey-independent growth of Bdellovibrio bacteriovorus HD100. J. Bacteriol. 193:71745–56 [Google Scholar]
  55. Sara M, Sleytr UB. 55.  2000. S-layer proteins. J. Bacteriol. 182:859–68 [Google Scholar]
  56. Schwudke D, Linscheid M, Strauch E, Appel B, Zahringer U. 56.  et al. 2003. The obligate predatory Bdellovibrio bacteriovorus possesses a neutral lipid A containing α-D-mannoses that replace phosphate residues: similarities and differences between the lipid As and the lipopolysaccharides of the wild type strain B. bacteriovorus HD100 and its host-independent derivative HI100. J. Biol. Chem. 278:27502–12 [Google Scholar]
  57. Shanks RM, Davra VR, Romanowski EG, Brothers KM, Stella NA. 57.  et al. 2013. An eye to a kill: using predatory bacteria to control gram-negative pathogens associated with ocular infections. PLOS ONE 8:e66723 [Google Scholar]
  58. Shatzkes K, Chae R, Tang C, Ramirez GC, Mukherjee S. 58.  et al. 2015. Examining the safety of respiratory and intravenous inoculation of Bdellovibrio bacteriovorus and Micavibrio aeruginosavorus in a mouse model. Sci. Rep. 5:12899 [Google Scholar]
  59. Shatzkes K, Connell ND, Kadouri DE. 59.  2017. Predatory bacteria: a new therapeutic approach for a post-antibiotic era. Future Microbiol 12:469–72 [Google Scholar]
  60. Shatzkes K, Singleton E, Tang C, Zuena M, Shukla S. 60.  et al. 2016. Predatory bacteria attenuate Klebsiella pneumoniae burden in rat lungs. mBio pii:e01847–16 [Google Scholar]
  61. Shemesh Y, Jurkevitch E. 61.  2004. Plastic phenotypic resistance to predation by Bdellovibrio and like organisms in bacterial prey. Environ. Microbiol. 6:12–18 [Google Scholar]
  62. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK. 62.  et al. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci. Transl. Med. 4:148ra16 [Google Scholar]
  63. Sockett RE, Lambert C. 63.  2004. Bdellovibrio as therapeutic agents: a predatory renaissance?. Nat. Rev. Microbiol. 2:669–75 [Google Scholar]
  64. Stewart PS, Costerton JW. 64.  2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135–38 [Google Scholar]
  65. Sutherland IW, Wilkinson JF. 65.  1965. Depolymerases for bacterial exopolysaccharides obtained from phage-infected bacteria. J. Gen. Microbiol. 39:373–83 [Google Scholar]
  66. Tudor JJ, Davis JJ, Panichella M, Zwolak A. 66.  2008. Isolation of predation-deficient mutants of Bdellovibrio bacteriovorus by using transposon mutagenesis. Appl. Environ. Microbiol. 74:5436–43 [Google Scholar]
  67. Tyson J, Sockett RE. 67.  2017. Nature knows best: employing whole microbial strategies to tackle antibiotic resistant pathogens. Environ. Microbiol. Rep. 9:147–49 [Google Scholar]
  68. Varon M, Fine M, Stein A. 68.  1984. The maintenance of Bdellovibrio at low prey density. Microb. Ecol. 10:95–98 [Google Scholar]
  69. Varon M, Shilo M. 69.  1968. Interaction of Bdellovibrio bacteriovorus and host bacteria. I. Kinetic studies of attachment and invasion of Escherichia coli B by Bdellovibrio bacteriovorus. J. Bacteriol. 95:744–53 [Google Scholar]
  70. Varon M, Shilo M. 70.  1969. Attachment of Bdellovibrio bacteriovorus to cell wall mutants of Salmonella spp. and Escherichia coli. J. Bacteriol. 95:744–53 [Google Scholar]
  71. Varon M, Zeigler BP. 71.  1978. Bacterial predator-prey interaction at low prey density. Appl. Environ. Microbiol. 36:11–17 [Google Scholar]
  72. Wall D. 72.  2016. Kin recognition in bacteria. Annu. Rev. Microbiol. 70:143–60 [Google Scholar]
  73. Westergaard JM, Kramer TT. 73.  1977. Bdellovibrio and the intestinal flora of vertebrates. Appl. Environ. Microbiol. 34:506–11 [Google Scholar]
  74. Wilkinson MHF. 74.  2001. Predation in the presence of decoys: an inhibitory factor on pathogen control by bacteriophages or bdellovibrios in dense and diverse ecosystems. J. Theor. Biol. 208:27–36 [Google Scholar]
  75. Willis AR, Moore C, Mazon-Moya M, Krokowski S, Lambert C. 75.  et al. 2016. Injections of predatory bacteria work alongside host immune cells to treat Shigella infection in zebrafish larvae. Curr. Biol. 26:3343–51 [Google Scholar]
/content/journals/10.1146/annurev-micro-090816-093618
Loading
Predator Versus Pathogen: How Does Predatory Bdellovibrio bacteriovorus Interface with the Challenges of Killing Gram-Negative Pathogens in a Host Setting?
Annual Review of Microbiology 71, 441 (2017); https://doi.org/10.1146/annurev-micro-090816-093618
/content/journals/10.1146/annurev-micro-090816-093618
/content/journals/10.1146/annurev-micro-090816-093618
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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