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Parallel genomics uncover novel enterococcal-bacteriophage interactions

Anushila Chatterjee, Julia L. E. Willett, Uyen Thy Nguyen, Brendan Monogue, View ORCID ProfileKelli L. Palmer, Gary M. Dunny, View ORCID ProfileBreck A. Duerkop
doi: https://doi.org/10.1101/858506
Anushila Chatterjee
Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, CO, USA, 80045.
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Julia L. E. Willett
Department of Microbiology and Immunology, University of Minnesota Medical School, Minneapolis, MN, USA, 55455.
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Uyen Thy Nguyen
Department of Biological Sciences, University of Texas at Dallas, Richardson, TX, USA, 75080.
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Brendan Monogue
Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, CO, USA, 80045.
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Kelli L. Palmer
Department of Biological Sciences, University of Texas at Dallas, Richardson, TX, USA, 75080.
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Gary M. Dunny
Department of Microbiology and Immunology, University of Minnesota Medical School, Minneapolis, MN, USA, 55455.
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Breck A. Duerkop
Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, CO, USA, 80045.
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  • ORCID record for Breck A. Duerkop
  • For correspondence: breck.duerkop@cuanschutz.edu
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Abstract

Bacteriophages (phages) have been proposed as alternative therapeutics for the treatment of multidrug resistant bacterial infections. However, there are major gaps in our understanding of the molecular events in bacterial cells that control how bacteria respond to phage predation. Using the model organism Enterococcus faecalis, we employed two distinct genomic approaches, transposon (Tn) library screening and RNA sequencing, to investigate the interaction of E. faecalis with a virulent phage. We discovered that a transcription factor encoding a LytR family response regulator controls the expression of enterococcal polysaccharide antigen (epa) genes that are involved in phage infection and bacterial fitness. In addition, we discovered that DNA mismatch repair mutants rapidly evolve phage adsorption deficiencies, underpinning a molecular basis for epa mutation during phage infection. Transcriptomic profiling of phage infected E. faecalis revealed broad transcriptional changes influencing viral replication and progeny burst size. We also demonstrate that phage infection alters the expression of bacterial genes associated with intra and inter-bacterial interactions, including genes involved in quorum sensing and polymicrobial competition. Together our results suggest that phage predation has the potential to influence complex microbial behavior and may dictate how bacteria respond to external environmental stimuli. These responses could have collateral effects (positive or negative) on microbial communities such as the host microbiota during phage therapy.

Importance We lack fundamental understanding of how phage infection influences bacterial gene expression and consequently how bacterial responses to phage infection affect the assembly of polymicrobial communities. Using parallel genomic approaches, we have discovered novel transcriptional regulators and metabolic genes that influence phage infection. The integration of whole genome transcriptomic profiling during phage infection has revealed the differential regulation of genes important for group behaviors and polymicrobial interactions. Our work suggests that therapeutic phages could more broadly influence bacterial community composition outside of their intended host targets.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 29, 2019.
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Parallel genomics uncover novel enterococcal-bacteriophage interactions
Anushila Chatterjee, Julia L. E. Willett, Uyen Thy Nguyen, Brendan Monogue, Kelli L. Palmer, Gary M. Dunny, Breck A. Duerkop
bioRxiv 858506; doi: https://doi.org/10.1101/858506
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Parallel genomics uncover novel enterococcal-bacteriophage interactions
Anushila Chatterjee, Julia L. E. Willett, Uyen Thy Nguyen, Brendan Monogue, Kelli L. Palmer, Gary M. Dunny, Breck A. Duerkop
bioRxiv 858506; doi: https://doi.org/10.1101/858506

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