1887

Microbiology Society logo

Volume 170, Issue 2

Predatory bacteria prevent the proliferation of intraocular and fluoroquinolone-resistant Open Access

Abstract

Endogenous endophthalmitis caused by Gram-negative bacteria is an intra-ocular infection that can rapidly progress to irreversible loss of vision. While most endophthalmitis isolates are susceptible to antibiotic therapy, the emergence of resistant bacteria necessitates alternative approaches to combat intraocular bacterial proliferation. In this study the ability of predatory bacteria to limit intraocular growth of , , and was evaluated in a New Zealand white rabbit endophthalmitis prevention model. Predatory bacteria and were able to reduce proliferation of keratitis isolates of and to a lesser extent . However, it was not able to significantly reduce the number of intraocular which is not a productive prey for these predatory bacteria, suggesting that the inhibitory effect on and requires active predation rather than an antimicrobial immune response. Similarly, UV-inactivated were unable to prevent proliferation of . Together, these data indicate inhibition of Gram-negative bacteria proliferation within the intra-ocular environment by predatory bacteria.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic resistance , Bdellovibrio bacteriovorus , endophthalmitis , infection , Micavibrio aeruginosavorus , ocular infection , predatory bacteria , Pseudomonas aeruginosa , Serratia marcescens and Staphylococcus aureus
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 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/micro/10.1099/mic.0.001433
2024-02-15
2024-05-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/2/mic001433.html?itemId=/content/journal/micro/10.1099/mic.0.001433&mimeType=html&fmt=ahah

References

  1. Dwidar M, Monnappa AK, Mitchell RJ. The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus. BMB Rep 2012; 45:71–78 [View Article] [PubMed]
     [Google Scholar]
  2. Negus D, Moore C, Baker M, Raghunathan D, Tyson J et al. Predator versus pathogen: how does predatory Bdellovibrio bacteriovorus interface with the challenges of killing Gram-negative pathogens in a host setting?. Annu Rev Microbiol 2017; 71:441–457 [View Article] [PubMed]
     [Google Scholar]
  3. Atterbury RJ, Tyson J. Predatory bacteria as living antibiotics - where are we now?. Microbiology 2021; 167: [View Article] [PubMed]
     [Google Scholar]
  4. Cavallo FM, Jordana L, Friedrich AW, Glasner C, van Dijl JM. Bdellovibrio bacteriovorus: a potential “living antibiotic” to control bacterial pathogens. Crit Rev Microbiol 2021; 47:630–646 [View Article] [PubMed]
     [Google Scholar]
  5. Dashiff A, Junka RA, Libera M, Kadouri DE. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. J Appl Microbiol 2011; 110:431–444 [View Article] [PubMed]
     [Google Scholar]
  6. Kadouri DE, To K, Shanks RMQ, Doi Y. Predatory bacteria: a potential ally against multidrug-resistant Gram-negative pathogens. PLoS One 2013; 8:e63397 [View Article] [PubMed]
     [Google Scholar]
  7. Dharani S, Kim DH, Shanks RMQ, Doi Y, Kadouri DE. Susceptibility of colistin-resistant pathogens to predatory bacteria. Res Microbiol 2018; 169:52–55 [View Article] [PubMed]
     [Google Scholar]
  8. Findlay JS, Flick-Smith HC, Keyser E, Cooper IA, Williamson ED et al. Predatory bacteria can protect SKH-1 mice from a lethal plague challenge. Sci Rep 2019; 9:7225 [View Article] [PubMed]
     [Google Scholar]
  9. Liu Y, Zhuang B, Yuan B, Zhang H, Li J et al. Predatory bacterial hydrogels for topical treatment of infected wounds. Acta Pharmaceutica Sinica B 2023; 13:315–326 [View Article]
     [Google Scholar]
  10. Maraş G, Ceyhan Ö, Türe Z, Sağıroğlu P, Yıldırım Y et al. The effect of Bdellovibrio bacteriovorus containing dressing on superficial incisional surgical site infections experimentally induced by Klebsiella pneumoniae in mice. J Tissue Viability 2023; 32:541–549 [View Article] [PubMed]
     [Google Scholar]
  11. Russo R, Kolesnikova I, Kim T, Gupta S, Pericleous A et al. Susceptibility of virulent Yersinia pestis bacteria to predator bacteria in the lungs of mice. Microorganisms 2018; 7:2 [View Article] [PubMed]
     [Google Scholar]
  12. Shatzkes K, Chae R, Tang C, Ramirez GC, Mukherjee S et al. Examining the safety of respiratory and intravenous inoculation of Bdellovibrio bacteriovorus and Micavibrio aeruginosavorus in a mouse model. Sci Rep 2015; 5:12899 [View Article] [PubMed]
     [Google Scholar]
  13. Shatzkes K, Singleton E, Tang C, Zuena M, Shukla S et al. Predatory bacteria attenuate Klebsiella pneumoniae burden in rat lungs. mBio 2016; 7:e01847–01816 [View Article] [PubMed]
     [Google Scholar]
  14. Silva PHF, Oliveira LFF, Cardoso RS, Santana SI, Casarin RC et al. Effects of Bdellovibrio bacteriovorus HD100 on experimental periodontitis in rats. Mol Oral Microbiol 2023; 38:158–170 [View Article] [PubMed]
     [Google Scholar]
  15. Tajabadi FH, Karimian SM, Mohsenipour Z, Mohammadi S, Salehi M et al. Biocontrol treatment: application of Bdellovibrio bacteriovorus HD100 against burn wound infection caused by Pseudomonas aeroginosa in mice. Burns 2023; 49:1181–1195 [View Article] [PubMed]
     [Google Scholar]
  16. Willis AR, Moore C, Mazon-Moya M, Krokowski S, Lambert C et al. Injections of predatory bacteria work alongside host immune cells to treat Shigella infection in zebrafish larvae. Curr Biol 2016; 26:3343–3351 [View Article] [PubMed]
     [Google Scholar]
  17. Cui M, Zheng M, Wiraja C, Chew SWT, Mishra A et al. Ocular delivery of predatory bacteria with cryomicroneedles against eye infection. Adv Sci 2021; 8:e2102327 [View Article] [PubMed]
     [Google Scholar]
  18. Romanowski EG, Gupta S, Pericleous A, Kadouri DE, Shanks RMQ. Clearance of Gram-Negative Bacterial Pathogens from the Ocular Surface by Predatory Bacteria. Antibiotics 2021; 10:810 [View Article]
     [Google Scholar]
  19. Romanowski EG, Stella NA, Brazile BL, Lathrop KL, Franks JM et al. Predatory bacteria can reduce Pseudomonas aeruginosa induced corneal perforation and proliferation in a rabbit keratitis model. Ocul Surf 2023; 28:254–261 [View Article] [PubMed]
     [Google Scholar]
  20. Boileau MJ, Mani R, Breshears MA, Gilmour M, Taylor JD et al. Efficacy of Bdellovibrio bacteriovorus 109J for the treatment of dairy calves with experimentally induced infectious bovine keratoconjunctivitis. Am J Vet Res 2016; 77:1017–1028 [View Article] [PubMed]
     [Google Scholar]
  21. Lee JY, Kim KH. Endogenous endophthalmitis complicated by pyogenic liver abscess: a review of 17 years’ experience at a single center. Digestion 2014; 90:116–121 [View Article] [PubMed]
     [Google Scholar]
  22. Tiecco G, Laurenda D, Mulè A, Arsuffi S, Storti S et al. Gram-negative endogenous endophthalmitis: a systematic review. Microorganisms 2022; 11:80 [View Article] [PubMed]
     [Google Scholar]
  23. Chen Y-J, Kuo H-K, Wu P-C, Kuo M-L, Tsai H-H et al. A 10-year comparison of endogenous endophthalmitis outcomes: an east Asian experience with Klebsiella pneumoniae infection. Retina 2004; 24:383–390 [View Article] [PubMed]
     [Google Scholar]
  24. Kowalski RP. The Charles T. Campbell Eye Microbiology Lab; 2023 https://eyemicrobiology.upmc.com/AntibioticSusceptibilities/Endophthalmitis.htm accessed 22 August 2023
  25. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 2004; 303:689–692 [View Article] [PubMed]
     [Google Scholar]
  26. Stolp H, Starr MP. Bdellovibrio bacteriovorus Gen. Et Sp. N., A predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 1963; 29:217–248 [View Article] [PubMed]
     [Google Scholar]
  27. Wang Z, Kadouri DE, Wu M. Genomic insights into an obligate epibiotic bacterial predator: Micavibrio aeruginosavorus ARL-13. BMC Genomics 2011; 12:453 [View Article] [PubMed]
     [Google Scholar]
  28. Gupta S, Tang C, Tran M, Kadouri DE. Effect of predatory bacteria on human cell lines. PLoS One 2016; 11:e0161242 [View Article] [PubMed]
     [Google Scholar]
  29. Caiazza NC, Lies DP, Newman DK. Phototrophic Fe(II) oxidation promotes organic carbon acquisition by Rhodobacter capsulatus SB1003. Appl Environ Microbiol 2007; 73:6150–6158 [View Article] [PubMed]
     [Google Scholar]
  30. Kowalski RP, Pandya AN, Karenchak LM, Romanowski EG, Husted RC et al. An in vitro resistance study of levofloxacin, ciprofloxacin, and ofloxacin using keratitis isolates of Staphylococcus aureus and Pseudomonas aeruginosa. Ophthalmology 2001; 108:1826–1829 [View Article] [PubMed]
     [Google Scholar]
  31. Kalivoda EJ, Stella NA, Aston MA, Fender JE, Thompson PP et al. Cyclic AMP negatively regulates prodigiosin production by Serratia marcescens. Res Microbiol 2010; 161:158–167 [View Article] [PubMed]
     [Google Scholar]
  32. Shanks RMQ, Davra VR, Romanowski EG, Brothers KM, Stella NA et al. An eye to a kill: using predatory bacteria to control Gram-negative pathogens associated with ocular infections. PLoS One 2013; 8:e66723 [View Article] [PubMed]
     [Google Scholar]
  33. Im H, Dwidar M, Mitchell RJ. Bdellovibrio bacteriovorus HD100, a predator of Gram-negative bacteria, benefits energetically from Staphylococcus aureus biofilms without predation. ISME J 2018; 12:2090–2095 [View Article] [PubMed]
     [Google Scholar]
  34. Lai TF, Ford RM, Huwiler SG. Advances in cellular and molecular predatory biology of Bdellovibrio bacteriovorus six decades after discovery. Front Microbiol 2023; 14:1168709 [View Article] [PubMed]
     [Google Scholar]
  35. Pasternak Z, Njagi M, Shani Y, Chanyi R, Rotem O et al. In and out: an analysis of epibiotic vs periplasmic bacterial predators. ISME J 2014; 8:625–635 [View Article] [PubMed]
     [Google Scholar]
  36. Fukuda K, Ishida W, Fukushima A, Nishida T. Corneal fibroblasts as sentinel cells and local immune modulators in infectious keratitis. Int J Mol Sci 2017; 18:1831 [View Article] [PubMed]
     [Google Scholar]
  37. Kumar A, Singh PK, Ahmed Z, Singh S, Kumar A. Essential role of NLRP3 inflammasome in mediating IL-1β production and the pathobiology of Staphylococcus aureus endophthalmitis. Infect Immun 2022; 90:e0010322 [View Article] [PubMed]
     [Google Scholar]
  38. Naik P, Joseph J. Temporal transcriptome analysis suggests modulation of key pathways and hub genes in a mice model of multi-drug resistant (MDR) Pseudomonas aeruginosa endophthalmitis. Curr Eye Res 2022; 47:1559–1566 [View Article] [PubMed]
     [Google Scholar]
  39. Petropoulos IK, Vantzou CV, Lamari FN, Karamanos NK, Anastassiou ED et al. Expression of TNF-α, IL-1β, and IFN-γ in Staphylococcus epidermidis slime-positive experimental endophthalmitis is closely related to clinical inflammatory scores. Graefe’s Arch Clin Exp Ophthalmo 2006; 244:1322–1328 [View Article]
     [Google Scholar]
  40. Monnappa AK, Bari W, Choi SY, Mitchell RJ. Investigating the responses of human epithelial cells to predatory bacteria. Sci Rep 2016; 6:33485 [View Article] [PubMed]
     [Google Scholar]
  41. Romanowski EG, Stella NA, Brothers KM, Yates KA, Funderburgh ML et al. Predatory bacteria are nontoxic to the rabbit ocular surface. Sci Rep 2016; 6:30987 [View Article] [PubMed]
     [Google Scholar]
  42. Shatzkes K, Tang C, Singleton E, Shukla S, Zuena M et al. Effect of predatory bacteria on the gut bacterial microbiota in rats. Sci Rep 2017; 7:43483 [View Article] [PubMed]
     [Google Scholar]
  43. Thomashow LS, Rittenberg SC. Isolation and composition of sheathed flagella from Bdellovibrio bacteriovorus 109J. J Bacteriol 1985; 163:1047–1054 [View Article] [PubMed]
     [Google Scholar]
  44. Schwudke D, Linscheid M, Strauch E, Appel B, Zahringer U et al. The obligate predatory Bdellovibrio bacteriovorus possesses a neutral lipid a containing alpha-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 2003; 278:27502–27512 [View Article] [PubMed]
     [Google Scholar]
  45. Miller FC, Coburn PS, Huzzatul MM, LaGrow AL, Livingston E et al. Targets of immunomodulation in bacterial endophthalmitis. Prog Retin Eye Res 2019; 73:100763 [View Article] [PubMed]
     [Google Scholar]
  46. Singh PK, Kumar A. Retinal photoreceptor expresses toll-like receptors (TLRs) and elicits innate responses following TLR ligand and bacterial challenge. PLoS One 2015; 10:e0119541 [View Article] [PubMed]
     [Google Scholar]
  47. Upatissa S, Mun W, Mitchell RJ. Pairing colicins B and E5 with Bdellovibrio bacteriovorus to eradicate carbapenem- and colistin-resistant strains of Escherichia coli. Microbiol Spectr 2023; 11:e0017323 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001433
Loading
Predatory bacteria prevent the proliferation of intraocular Serratia marcescens and fluoroquinolone-resistant Pseudomonas aeruginosa
Microbiology 170, 001433 (2024); https://doi.org/10.1099/mic.0.001433
/content/journal/micro/10.1099/mic.0.001433
/content/journal/micro/10.1099/mic.0.001433
Loading

Data & Media loading...

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