TY - JOUR
T1 - Dual predation by bacteriophage and Bdellovibrio bacteriovorus can eradicate Escherichia coli prey in situations where single predation cannot
AU - Hobley, Laura
AU - Summers, J. Kimberley
AU - Till, Rob
AU - Milner, David S.
AU - Atterbury, Robert J.
AU - Stroud, Amy
AU - Capeness, Michael J.
AU - Gray, Stephanie
AU - Leidenroth, Andreas
AU - Lambert, Carey
AU - Connerton, Ian
AU - Twycross, Jamie
AU - Baker, Michelle
AU - Tyson, Jess
AU - Kreft, Jan-Ulrich
AU - Sockett, R. Elizabeth
PY - 2020/2/25
Y1 - 2020/2/25
N2 - 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.
AB - 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.
KW - Approximate Bayesian computation
KW - Bacteriophage
KW - Bdellovibrio
KW - Cooperation
KW - Cooperation
KW - Mathematical modeling
KW - Predation
KW - Predator prey models
KW - Predator-prey models
KW - RTP phage
UR - http://www.scopus.com/inward/record.url?scp=85083899052&partnerID=8YFLogxK
U2 - 10.1128/JB.00629-19
DO - 10.1128/JB.00629-19
M3 - Article
C2 - 31907203
SN - 0021-9193
VL - 202
SP - 1
EP - 18
JO - Journal of Bacteriology
JF - Journal of Bacteriology
IS - 6
M1 - e00629-19
ER -