Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation
Open Access
- 8 March 2017
- journal article
- Published by American Society for Microbiology in mBio
- Vol. 8 (1), e02115-16
- https://doi.org/10.1128/mbio.02115-16
Abstract
Bacteriophages infect an estimated 1023 to 1025 bacterial cells each second, many of which carry physiologically relevant plasmids (e.g., those encoding antibiotic resistance). However, even though phage-plasmid interactions occur on a massive scale and have potentially significant evolutionary, ecological, and biomedical implications, plasmid fate upon phage infection and lysis has not been investigated to date. Here we show that a subset of the natural lytic phage population, which we dub “superspreaders,” releases substantial amounts of intact, transformable plasmid DNA upon lysis, thereby promoting horizontal gene transfer by transformation. Two novel Escherichia coli phage superspreaders, SUSP1 and SUSP2, liberated four evolutionarily distinct plasmids with equal efficiency, including two close relatives of prominent antibiotic resistance vectors in natural environments. SUSP2 also mediated the extensive lateral transfer of antibiotic resistance in unbiased communities of soil bacteria from Maryland and Wyoming. Furthermore, the addition of SUSP2 to cocultures of kanamycin-resistant E. coli and kanamycin-sensitive Bacillus sp. bacteria resulted in roughly 1,000-fold more kanamycin-resistant Bacillus sp. bacteria than arose in phage-free controls. Unlike many other lytic phages, neither SUSP1 nor SUSP2 encodes homologs to known hydrolytic endonucleases, suggesting a simple potential mechanism underlying the superspreading phenotype. Consistent with this model, the deletion of endonuclease IV and the nucleoid-disrupting protein ndd from coliphage T4, a phage known to extensively degrade chromosomal DNA, significantly increased its ability to promote plasmid transformation. Taken together, our results suggest that phage superspreaders may play key roles in microbial evolution and ecology but should be avoided in phage therapy and other medical applications.This publication has 52 references indexed in Scilit:
- Complete Genome Sequence of Bacteriophage EC6, Capable of Lysing Escherichia coli O157:H7Microbiology Resource Announcements, 2013
- Antibiotics and UV Radiation Induce Competence for Natural Transformation inLegionella pneumophilaJournal of Bacteriology, 2011
- Use of Ichip for High-Throughput In Situ Cultivation of “Uncultivable” Microbial SpeciesApplied and Environmental Microbiology, 2010
- Integration of stable extracellular DNA released from Escherichia coli into the Bacillus subtilis genome vector by culture mix methodNucleic Acids Research, 2010
- Functional viral metagenomics and the next generation of molecular toolsTrends in Microbiology, 2010
- Replication and conjugative mobilization of broad host-range IncQ plasmidsPlasmid, 2009
- DNAPlotter: circular and linear interactive genome visualizationBioinformatics, 2008
- Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteriaBritish Journal of Pharmacology, 2008
- Mechanisms of, and Barriers to, Horizontal Gene Transfer between BacteriaNature Reviews Microbiology, 2005
- The Complete Genome Sequence of Escherichia coli K-12Science, 1997