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.2016 Nov 7:7:13333.
doi: 10.1038/ncomms13333.

Bacterial viruses enable their host to acquire antibiotic resistance genes from neighbouring cells

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Bacterial viruses enable their host to acquire antibiotic resistance genes from neighbouring cells

Jakob Haaber et al. Nat Commun..

Abstract

Prophages are quiescent viruses located in the chromosomes of bacteria. In the human pathogen, Staphylococcus aureus, prophages are omnipresent and are believed to be responsible for the spread of some antibiotic resistance genes. Here we demonstrate that release of phages from a subpopulation of S. aureus cells enables the intact, prophage-containing population to acquire beneficial genes from competing, phage-susceptible strains present in the same environment. Phage infection kills competitor cells and bits of their DNA are occasionally captured in viral transducing particles. Return of such particles to the prophage-containing population can drive the transfer of genes encoding potentially useful traits such as antibiotic resistance. This process, which can be viewed as 'auto-transduction', allows S. aureus to efficiently acquire antibiotic resistance both in vitro and in an in vivo virulence model (wax moth larvae) and enables it to proliferate under strong antibiotic selection pressure. Our results may help to explain the rapid exchange of antibiotic resistance genes observed in S. aureus.

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Figures

Figure 1
Figure 1. Phages transfer DNA from non-lysogenic cells back to the lysogenic host.
(a) Frequencies of double or triple resistant cells of total CFU when co-culturing strains 8325-4 SaPI, 8325-4 plasmid, 8325-4 chrom and the non-marker control 8325-4 with 8325-S (filled bars) or 8325-SR (open bars), respectively. No double or triple resistant cells were observed when the lysogen was substituted with the phage-cured derivatives JH977 or JH978 (detection limit=4e−10). (b) Haemolysis phenotype of parental strains 8325-S (lysogen), 8325-4 (non-lysogen) carrying SaPI, plasmid or chromosomal markers, and double resistant colonies obtained from co-cultures shown ina (scale bar, 10 mm). (c) Frequencies of double resistant cells in cultures where 8325-S and phage-susceptible 8325-4 SaPI populations were grown separately but sequentially exposed to sterile-filtered culture supernatant and in presence of DNase or citrate, the latter of which binds Ca2+ (see Methods and Supplementary Fig. 4 for details of experimental setup). (d) Frequencies of double resistant CFU in co-cultures of 8325-4 SaPI (filled bars) or 8325-4 plasmid (open bars) and streptomycin-resistant lysogens harbouring a wild-type phage (Φ11) or derived phage mutants (Φ11 CI and Φ11 terL). For frequency of spontaneous antibiotic resistance development, see Supplementary Table 3. Error bars=s.d.,n=3. ***P<0.001,**P<0.01 and *P<0.05, NS, not significant (t-test).
Figure 2
Figure 2. Acquisition of foreign DNA by lysogenic and non-lysogenic strains.
Lysogenic 8325-SR (black bars) and non-lysogenic JH978 (grey bars) strains were exposed for 24 h to a phage lysate obtained from 8325-4 SaPI at MOI=0.1 (a) or 1 (b) after which the total number of bacteria, transductants and phages were determined by plating without (bacteria) and with antibiotic selection (transductants) or by spotting for phage titers (phage). Error bars=s.d.,n=3. ***P<0.001 (t-test).
Figure 3
Figure 3. Autotransduction occurs without and with antibiotic selection.
(a) At time zero, lysogenic 8325-SR (circles) was spotted on agar plates without antibiotics containing a growing USA300 population (squares) forming autotransduced 8325-SR (triangles). At selected time points, equal size areas of the agar were stamped out, cells extracted and plated on blood agar plates containing the relevant antibiotics. (b,c) Percentage lysogen (8325-SR) in liquid co-cultures with phage susceptible but erythromycin-resistant 8325-4 chrom (b) or USA300 (c) grown in the presence of erythromycin with (open bars) or without citrate (black bars). Percentage autotransductants of total population in the absence on citrate (grey bars) plotted on log-scale axis. No autotransductants were obtained in cultures with citrate. Error bars=s.d.,n=3.
Figure 4
Figure 4. Autotransduction occurs in anin vivo infection model.
Autotransduction frequencies recorded over time during co-infection ofG. mellonella larvae with 8325-SR and (a) 8325-4 SaPI or (b) USA300. At each time point, 20 larvae were sampled and total CFU and triple-resistant colonies were determined from the haemolymph. The calculated autotransduction frequencies are shown for the larvae in which autotransduction was observed. Filled and open symbols represent living and dead larvae, respectively. No autotransduction was observed in the inoculum used for infection; when lysogenic bacteria were substituted with a phage-cured derivative (JH978); when the non-lysogenic strain was substituted with 8325-4 not carrying an antibiotic resistance marker or when larvae were injected with a PBS control (detection limit=2e−9).
Figure 5
Figure 5. Autotransduction model.
(A) Spontaneous phage induction mediated by RecA cleavage of the CI phage repressor from a subpopulation of a lysogenic bacterial population allows the phage to infect a susceptible co-existing bacterial population. (B) Propagation on the susceptible population and subsequent lysis releases phage progeny along with low numbers of transducing particles. (C) Owing to immunity to its own phages, the lysogenic population can ‘filter out' the infective phage progeny and allow the occasional transducing particle to deliver its DNA to the lysogenic population by autotransduction.
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