title: The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin.
abstract: The viral population, including bacteriophages, is an important component of the human microbiota, yet is poorly understood. We aim to determine whether bacteriophages modulate the composition of the bacterial populations, thus potentially playing a role in health or disease. We investigated the diversity and host interactions of the bacteriophages of Propionibacterium acnes, a major human skin commensal implicated in acne pathogenesis. By sequencing 48 P. acnes phages isolated from acne patients and healthy individuals and by analyzing the P. acnes phage populations in healthy skin metagenomes, we revealed that P. acnes phage populations in the skin microbial community are often dominated by one strain. We also found phage strains shared among both related and unrelated individuals, suggesting that a pool of common phages exists in the human population and that transmission of phages may occur between individuals. To better understand the bacterium-phage interactions in the skin microbiota, we determined the outcomes of 74 genetically defined Propionibacterium strains challenged by 15 sequenced phages. Depending on the Propionibacterium lineage, phage infection can result in lysis, pseudolysogeny, or resistance. In type II P. acnes strains, we found that encoding matching clustered regularly interspaced short palindromic repeat spacers is insufficient to confer phage resistance. Overall, our findings suggest that the prey-predator relationship between bacteria and phages may have a role in modulating the composition of the microbiota. Our study also suggests that the microbiome structure of an individual may be an important factor in the design of phage-based therapy.
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Jared
authors.initials: J
authors.lastname: Liu
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Riceley
authors.initials: R
authors.lastname: Yan
authors.affiliation: 1] Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA [2] Department of Laboratory Medicine, Suzhou Municipal Hospital, Suzhou Hospital Affiliated to Nanjing Medical University, Suzhou, China.
authors.forename: Qiao
authors.initials: Q
authors.lastname: Zhong
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Sam
authors.initials: S
authors.lastname: Ngo
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Nathanael J
authors.initials: NJ
authors.lastname: Bangayan
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Lin
authors.initials: L
authors.lastname: Nguyen
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Timothy
authors.initials: T
authors.lastname: Lui
authors.affiliation: Department of Microbiology, Immunology and Molecular Genetics, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Minghsun
authors.initials: M
authors.lastname: Liu
authors.affiliation: Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Los Angeles, CA, USA.
authors.forename: Marie C
authors.initials: MC
authors.lastname: Erfe
authors.affiliation: Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Los Angeles, CA, USA.
authors.forename: Noah
authors.initials: N
authors.lastname: Craft
authors.affiliation: Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA.
authors.forename: Shuta
authors.initials: S
authors.lastname: Tomida
authors.affiliation: 1] Department of Molecular and Medical Pharmacology, Crump Institute for Molecular Imaging, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA [2] UCLA-DOE Institute for Genomics and Proteomics, Los Angeles, CA, USA.
authors.forename: Huiying
authors.initials: H
authors.lastname: Li
mesh_terms: D000152:Acne Vulgaris / Q000382:microbiology*; D001435:Bacteriophages / Q000235:genetics*; D001483:Base Sequence; D044822:Biodiversity; D064112:Clustered Regularly Interspaced Short Palindromic Repeats; D016679:Genome, Viral; D054884:Host-Pathogen Interactions; D006801:Humans; D054892:Metagenome; D008854:Microscopy, Electron; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide; D011425:Propionibacterium acnes / Q000235:genetics* / Q000472:pathogenicity* / Q000821:virology; D012867:Skin / Q000382:microbiology*
references.citation: PLoS One. 2012;7(6):e38499
references.pmid: 22723863
references.citation: PLoS One. 2010 Aug 19;5(8):e12277
references.pmid: 20808860
references.citation: Microbiology (Reading). 1997 Jun;143(6):2065-2070
references.pmid: 33711876
references.citation: Cell. 2003 Apr 18;113(2):141
references.pmid: 12705861
references.citation: J Clin Microbiol. 2010 Oct;48(10):3575-81
references.pmid: 20702672
references.citation: Nature. 2012 Jun 13;486(7402):207-14
references.pmid: 22699609
references.citation: Clin Dermatol. 2004 Sep-Oct;22(5):375-9
references.pmid: 15556721
references.citation: Med Microbiol Immunol. 1975 Sep 19;161(4):263-71
references.pmid: 1196261
references.citation: Proc Natl Acad Sci U S A. 2005 Nov 29;102(48):17472-7
references.pmid: 16287978
references.citation: Genome Announc. 2013 Jun 27;1(3):
references.pmid: 23792747
references.citation: J Am Acad Dermatol. 1998 Aug;39(2 Pt 3):S34-7
references.pmid: 9703121
references.citation: Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W157-62
references.pmid: 18515345
references.citation: J Invest Dermatol. 2013 Sep;133(9):2152-60
references.pmid: 23337890
references.citation: Science. 2009 May 29;324(5931):1190-2
references.pmid: 19478181
references.citation: Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
references.pmid: 12136088
references.citation: Microbiology (Reading). 2009 Mar;155(Pt 3):733-740
references.pmid: 19246744
references.citation: Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12450-5
references.pmid: 23836644
references.citation: Environ Microbiol. 2012 Sep;14(9):2526-37
references.pmid: 22713159
references.citation: BMC Biol. 2014 Sep 10;12:71
references.pmid: 25212266
references.citation: Genome Biol. 2004;5(2):R12
references.pmid: 14759262
references.citation: Appl Environ Microbiol. 2012 Jun;78(12):4510-5
references.pmid: 22504803
references.citation: Nucleic Acids Res. 1999 Dec 1;27(23):4636-41
references.pmid: 10556321
references.citation: Virol J. 2006 May 23;3:30
references.pmid: 16716236
references.citation: FEMS Microbiol Lett. 2009 Jul;296(1):110-6
references.pmid: 19459963
references.citation: Genome Res. 1998 Mar;8(3):195-202
references.pmid: 9521923
references.citation: Virology. 2012 Dec 20;434(2):181-6
references.pmid: 23084423
references.citation: Science. 2006 Jan 27;311(5760):496-503
references.pmid: 16439655
references.citation: J Clin Microbiol. 1976 Aug;2(2):104-10
references.pmid: 972178
references.citation: Virology. 2012 Dec 20;434(2):187-201
references.pmid: 23084079
references.citation: Appl Environ Microbiol. 1993 Oct;59(10):3393-9
references.pmid: 16349072
references.citation: Genome Announc. 2014 Aug 14;2(4):
references.pmid: 25125638
references.citation: J Bacteriol. 2009 Dec;191(23):7206-15
references.pmid: 19783628
references.citation: Nature. 2013 Jan 17;493(7432):429-32
references.pmid: 23242138
references.citation: Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10098-103
references.pmid: 21646539
references.citation: ISME J. 2013 Jan;7(1):85-95
references.pmid: 22895161
references.citation: Nature. 2013 Jun 20;498(7454):367-70
references.pmid: 23698366
references.citation: Br J Dermatol. 1979 Nov;101(5):543-8
references.pmid: 160242
references.citation: J Virol. 2014 May;88(9):4786-97
references.pmid: 24522917
references.citation: Science. 2010 Jan 8;327(5962):167-70
references.pmid: 20056882
references.citation: J Invest Dermatol. 1973 Feb;60(2):80-3
references.pmid: 4266324
references.citation: ISME J. 2012 May;6(5):915-26
references.pmid: 22158393
references.citation: Mol Biol Evol. 2011 Oct;28(10):2731-9
references.pmid: 21546353
references.citation: Nature. 2009 May 14;459(7244):207-12
references.pmid: 19444207
references.citation: mBio. 2012 Oct 30;3(6):
references.pmid: 23111870
references.citation: BMC Genomics. 2013 May 10;14:320
references.pmid: 23663384
references.citation: Mol Cell. 2012 Jun 8;46(5):595-605
references.pmid: 22521689
references.citation: Semin Cutan Med Surg. 2001 Sep;20(3):139-43
references.pmid: 11594668
references.citation: mBio. 2012 Sep 25;3(5):
references.pmid: 23015740
references.citation: Proc Natl Acad Sci U S A. 2007 Feb 20;104(8):2927-32
references.pmid: 17293459
references.citation: Postepy Dermatol Alergol. 2013 Jun;30(3):178-87
references.pmid: 24278071
references.citation: Acta Pathol Microbiol Scand. 1964;60:599-608
references.pmid: 14154722
references.citation: FEMS Yeast Res. 2008 May;8(3):460-71
references.pmid: 18294199
references.citation: Nucleic Acids Res. 1998 Feb 15;26(4):1107-15
references.pmid: 9461475
references.citation: BMC Genomics. 2011 Apr 19;12:198
references.pmid: 21504575
references.citation: J Bacteriol. 2011 May;193(10):2460-7
references.pmid: 21421763
references.citation: mBio. 2013 Apr 30;4(3):e00003-13
references.pmid: 23631911
references.citation: Science. 2011 Jul 1;333(6038):58-62
references.pmid: 21719670
references.citation: Nat Rev Microbiol. 2009 Nov;7(11):828-36
references.pmid: 19834481
references.citation: Science. 2009 Dec 18;326(5960):1694-7
references.pmid: 19892944
references.citation: Genome Res. 2012 May;22(5):850-9
references.pmid: 22310478
references.citation: J Allergy Clin Immunol. 2012 May;129(5):1204-8
references.pmid: 22541361
references.citation: PLoS One. 2010 Jun 15;5(6):e11126
references.pmid: 20559554
references.citation: J Clin Microbiol. 1978 Jan;7(1):84-90
references.pmid: 624772
references.citation: PLoS One. 2012;7(7):e41480
references.pmid: 22859988
references.citation: Bioinformatics. 2000 Oct;16(10):944-5
references.pmid: 11120685
references.citation: mBio. 2014 Apr 15;5(2):e00896
references.pmid: 24736222
references.citation: Environ Microbiol. 2013 Aug;15(8):2306-18
references.pmid: 23489642
references.citation: Microbiology (Reading). 1998 Aug;144 ( Pt 8):2225-2232
references.pmid: 9720044
references.citation: PLoS Genet. 2013;9(12):e1003987
references.pmid: 24348267
references.citation: J Bacteriol. 2011 Jul;193(14):3678
references.pmid: 21571999
references.citation: Nucleic Acids Res. 2013 Dec;41(22):10509-17
references.pmid: 24021627
references.citation: J Bacteriol. 2007 Jun;189(11):4161-7
references.pmid: 17400737
references.citation: Nat Commun. 2013;4:1431
references.pmid: 23385576