Abstract
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.
Highlights
Bacteria are preyed upon by diverse microbial predators, including bacteriophage and predatory bacteria, such as Bdellovibrio bacteriovorus
Sequencing and alignment of the 16S rRNA gene amplified from predatory Bdellovibrio purified from a single isolated “haloed” plaque showed that the Bdellovibrio was a member of the B. bacteriovorus species, and its 16S rRNA sequence
When attempting to isolate Bdellovibrio strains from environmental sources, a sample of chicken farm wastewater gave haloed plaques on lawns of E. coli due to the combined predation by the new strain of B. bacteriovorus, which we named angelus, and an RTP-like bacteriophage, which we named halo
Summary
Bacteria are preyed upon by diverse microbial predators, including bacteriophage and predatory bacteria, such as Bdellovibrio bacteriovorus. 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. Bacteriophage are obligate intracellular predators that can be found in environments wherever susceptible bacteria are available; more than 95% of phage isolates described to date belong to the order Caudovirales or “tailed phage” [13] The tails of these phage attach to receptors on the surface of the host bacterium, including flagella [14], lipopolysaccharide [15], or outer membrane proteins [16]. Host resistance against bacteriophage infection falls within four general categories: inhibition of adsorption, blocking injection of the viral genome, recognition and restriction modification of bacterial DNA, and inhibition of the transcription and replication of phage DNA [18, 19]
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