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Dual predation by bacteriophage and bdellovibrio bacteriovorus can eradicate escherichia coli prey in situations where single predation cannot

Hobley, Laura; Summers, J. Kimberley; Till, Rob; Milner, David S.; Atterbury, Robert J.; Stroud, Amy; Capeness, Michael J.; Gray, Stephanie; Leidenroth, Andreas; Lambert, Carey; Connerton, Ian; Twycross, Jamie; Baker, Michelle; Tyson, Jess; Kreft, Jan Ulrich; Sockett, R. Elizabeth

Dual predation by bacteriophage and bdellovibrio bacteriovorus can eradicate escherichia coli prey in situations where single predation cannot Thumbnail


Authors

J. Kimberley Summers

Rob Till

David S. Milner

Amy Stroud

Michael J. Capeness

Stephanie Gray

Andreas Leidenroth

IAN CONNERTON IAN.CONNERTON@NOTTINGHAM.AC.UK
Northern Foods Professor of Food Safety

Jess Tyson

Jan Ulrich Kreft



Abstract

Copyright © 2020 Hobley et al. Bacteria are preyed upon by diverse microbial predators, including bacteriophage and predatory bacteria, such as Bdellovibrio bacteriovorus. While bacteriophage are used as antimicrobial therapies in Eastern Europe and are being applied for compassionate use in the United States, predatory bacteria are only just beginning to reveal their potential therapeutic uses. However, predation by either predator type can falter due to different adaptations arising in the prey bacteria. When testing poultry farm wastewater for novel Bdellovibrio isolates on Escherichia coli prey lawns, individual composite plaques were isolated containing both an RTP (rosette-tailed-phage)-like-phage and a B. bacteriovorus strain and showing central prey lysis and halos of extra lysis. Combining the purified phage with a lab strain of B. bacteriovorus HD100 recapitulated haloed plaques and increased killing of the E. coli prey in liquid culture, showing an effective side-by-side action of these predators compared to their actions alone. Using approximate Bayesian computation to select the best fitting from a variety of different mathematical models demonstrated that the experimental data could be explained only by assuming the existence of three prey phenotypes: (i) sensitive to both predators, (ii) genetically resistant to phage only, and (iii) plastic resistant to B. bacteriovorus only. Although each predator reduces prey availability for the other, high phage numbers did not abolish B. bacteriovorus predation, so both predators are competent to coexist and are causing different selective pressures on the bacterial surface while, in tandem, controlling prey bacterial numbers efficiently. This suggests that combinatorial predator therapy could overcome problems of phage resistance. Importance: With increasing levels of antibiotic resistance, the development of alternative antibacterial therapies is urgently needed. Two potential alternatives are bacteriophage and predatory bacteria. Bacteriophage therapy has been used, but prey/host specificity and the rapid acquisition of bacterial resistance to bacteriophage are practical considerations. Predatory bacteria are of interest due to their broad Gram-negative bacterial prey range and the lack of simple resistance mechanisms. Here, a bacteriophage and a strain of Bdellovibrio bacteriovorus, preyed side by side on a population of E. coli, causing a significantly greater decrease in prey numbers than either alone. Such combinatorial predator therapy may have greater potential than individual predators since prey surface changes selected for by each predator do not protect prey against the other predator.

Citation

Hobley, L., Summers, J. K., Till, R., Milner, D. S., Atterbury, R. J., Stroud, A., …Sockett, R. E. (2020). Dual predation by bacteriophage and bdellovibrio bacteriovorus can eradicate escherichia coli prey in situations where single predation cannot. Journal of Bacteriology, 202(6), Article e00629-19. https://doi.org/10.1128/JB.00629-19

Journal Article Type Article
Acceptance Date Dec 17, 2019
Online Publication Date Jan 6, 2020
Publication Date Jan 6, 2020
Deposit Date Jan 9, 2020
Publicly Available Date Mar 29, 2024
Journal Journal of Bacteriology
Print ISSN 0021-9193
Electronic ISSN 1098-5530
Publisher American Society for Microbiology
Peer Reviewed Peer Reviewed
Volume 202
Issue 6
Article Number e00629-19
DOI https://doi.org/10.1128/JB.00629-19
Keywords Molecular Biology; Microbiology
Public URL https://nottingham-repository.worktribe.com/output/3696668
Publisher URL https://jb.asm.org/content/early/2020/01/02/JB.00629-19

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