The host phylogeny determines viral infectivity and replication across Staphylococcus host species.
Journal
PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
08
12
2022
accepted:
18
05
2023
revised:
21
06
2023
medline:
23
6
2023
pubmed:
8
6
2023
entrez:
8
6
2023
Statut:
epublish
Résumé
Virus host shifts, where a virus transmits to and infects a novel host species, are a major source of emerging infectious disease. Genetic similarity between eukaryotic host species has been shown to be an important determinant of the outcome of virus host shifts, but it is unclear if this is the case for prokaryotes where anti-virus defences can be transmitted by horizontal gene transfer and evolve rapidly. Here, we measure the susceptibility of 64 strains of Staphylococcaceae bacteria (48 strains of Staphylococcus aureus and 16 non-S. aureus species spanning 2 genera) to the bacteriophage ISP, which is currently under investigation for use in phage therapy. Using three methods-plaque assays, optical density (OD) assays, and quantitative (q)PCR-we find that the host phylogeny explains a large proportion of the variation in susceptibility to ISP across the host panel. These patterns were consistent in models of only S. aureus strains and models with a single representative from each Staphylococcaceae species, suggesting that these phylogenetic effects are conserved both within and among host species. We find positive correlations between susceptibility assessed using OD and qPCR and variable correlations between plaque assays and either OD or qPCR, suggesting that plaque assays alone may be inadequate to assess host range. Furthermore, we demonstrate that the phylogenetic relationships between bacterial hosts can generally be used to predict the susceptibility of bacterial strains to phage infection when the susceptibility of closely related hosts is known, although this approach produced large prediction errors in multiple strains where phylogeny was uninformative. Together, our results demonstrate the ability of bacterial host evolutionary relatedness to explain differences in susceptibility to phage infection, with implications for the development of ISP both as a phage therapy treatment and as an experimental system for the study of virus host shifts.
Identifiants
pubmed: 37289828
doi: 10.1371/journal.ppat.1011433
pii: PPATHOGENS-D-22-02121
pmc: PMC10284401
doi:
Banques de données
figshare
['10.6084/m9.figshare.21642209.v1']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1011433Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M009122/1
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 109385/Z/15/Z
Pays : United Kingdom
Informations de copyright
Copyright: © 2023 Walsh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Infect Immun. 1979 Feb;23(2):549-52
pubmed: 154475
Nat Commun. 2021 Nov 29;12(1):6965
pubmed: 34845206
Nat Commun. 2022 Jan 18;13(1):372
pubmed: 35042853
Nature. 2009 Jun 25;459(7250):1122-5
pubmed: 19516283
Evolution. 2003 Mar;57(3):544-57
pubmed: 12703944
Antimicrob Agents Chemother. 2005 Mar;49(3):1220-1
pubmed: 15728933
Virology. 2006 Jun 20;350(1):146-57
pubmed: 16643978
Nature. 2008 Feb 21;451(7181):990-3
pubmed: 18288193
mSphere. 2021 Jan 13;6(1):
pubmed: 33441407
Lancet. 2006 Dec 23;368(9554):2211-8
pubmed: 17189032
J Bacteriol. 2006 Aug;188(15):5578-85
pubmed: 16855248
J Infect Dis. 2003 Feb 15;187(4):613-24
pubmed: 12599078
Viruses. 2020 Sep 26;12(10):
pubmed: 32993161
Microbiology (Reading). 1998 Sep;144 ( Pt 9):2469-2479
pubmed: 9782494
Philos Trans R Soc Lond B Biol Sci. 2012 Oct 19;367(1604):2864-71
pubmed: 22966141
ISME J. 2016 Dec;10(12):2854-2866
pubmed: 27258950
Nucleic Acids Res. 2014;42(16):10618-31
pubmed: 25120263
Mol Biol Evol. 2006 Jan;23(1):7-9
pubmed: 16177232
Front Cell Infect Microbiol. 2012 Feb 08;2:6
pubmed: 22919598
Am Nat. 2002 Dec;160(6):712-26
pubmed: 18707460
Nat Rev Microbiol. 2013 Oct;11(10):675-87
pubmed: 23979432
Biol Lett. 2012 Oct 23;8(5):829-32
pubmed: 22628096
PLoS Pathog. 2015 Mar 16;11(3):e1004728
pubmed: 25774803
J Bacteriol. 1971 Oct;108(1):584-5
pubmed: 4256428
Nat Med. 2020 Apr;26(4):450-452
pubmed: 32284615
World J Gastrointest Pharmacol Ther. 2017 Aug 6;8(3):162-173
pubmed: 28828194
Nucleic Acids Res. 2013 Apr;41(8):4360-77
pubmed: 23470997
Med Microbiol Immunol. 1988;177(4):229-33
pubmed: 2971134
J Bacteriol. 2017 Jul 25;199(16):
pubmed: 28559294
Nature. 2014 Apr 10;508(7495):254-7
pubmed: 24531761
J Evol Biol. 2009 Dec;22(12):2532-41
pubmed: 19878406
J Infect Dis. 1987 Apr;155(4):812-5
pubmed: 3102633
Emerg Infect Dis. 2005 Dec;11(12):1842-7
pubmed: 16485468
Bioinformatics. 2019 Feb 1;35(3):526-528
pubmed: 30016406
Science. 2018 Nov 2;362(6414):577-580
pubmed: 30385576
PLoS Biol. 2021 Sep 28;19(9):e3001390
pubmed: 34582436
Mol Biol Evol. 2022 Aug 06;:
pubmed: 35932227
Philos Trans R Soc Lond B Biol Sci. 2001 Dec 29;356(1416):1817-28
pubmed: 11779380
Infect Immun. 1999 Oct;67(10):5427-33
pubmed: 10496925
Proc Natl Acad Sci U S A. 2020 Nov 17;117(46):28859-28866
pubmed: 33122433
Proc Biol Sci. 2023 Jan 25;290(1991):20222237
pubmed: 36651046
Methods Mol Biol. 2016;1373:9-23
pubmed: 25646604
Appl Environ Microbiol. 2014 Nov;80(21):6694-703
pubmed: 25149517
Nat Rev Microbiol. 2020 Feb;18(2):113-119
pubmed: 31695182
Bacteriophage. 2011 Mar;1(2):86-93
pubmed: 22334864
PLoS One. 2016 Aug 03;11(8):e0160242
pubmed: 27487020
Mol Biol Evol. 2012 Aug;29(8):1969-73
pubmed: 22367748
Nature. 1999 Oct 28;401(6756):877-84
pubmed: 10553904
Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11954-8
pubmed: 20547849
Philos Trans R Soc Lond B Biol Sci. 2021 Nov 8;376(1837):20200358
pubmed: 34538140
Science. 2007 Mar 23;315(5819):1709-12
pubmed: 17379808
J Virol. 2008 Nov;82(22):11096-105
pubmed: 18768982
Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5174-9
pubmed: 15788529
Elife. 2021 Jan 08;10:
pubmed: 33416498
mBio. 2023 Apr 25;14(2):e0249022
pubmed: 36779718
PLoS Pathog. 2011 Sep;7(9):e1002260
pubmed: 21966271
Front Cell Infect Microbiol. 2012 Apr 12;2:49
pubmed: 22919640
Am Nat. 2004 Jan;163(1):84-96
pubmed: 14767838
Philos Trans R Soc Lond B Biol Sci. 2010 Aug 27;365(1552):2487-94
pubmed: 20643738
Cell. 2021 Sep 16;184(19):4848-4856
pubmed: 34480864
J Bacteriol. 2011 Aug;193(15):4006-9
pubmed: 21642458
Sci Rep. 2019 Sep 25;9(1):13893
pubmed: 31554892
Science. 2010 Aug 6;329(5992):676-9
pubmed: 20689015
Retrovirology. 2006 Jan 06;3:2
pubmed: 16398936
J Bacteriol. 2004 Apr;186(8):2430-8
pubmed: 15060046
Evolution. 2009 Mar;63(3):624-40
pubmed: 19054050
J Bacteriol. 2012 Sep;194(18):5012-9
pubmed: 22797755
Appl Environ Microbiol. 2011 Feb;77(3):756-61
pubmed: 21148689
Biomol Detect Quantif. 2015 Jul 30;5:10-4
pubmed: 27077038
PLoS One. 2009;4(3):e4944
pubmed: 19300511
Infect Immun. 2000 Sep;68(9):5205-9
pubmed: 10948145
Virology. 1974 Dec;62(2):367-84
pubmed: 4610993
Annu Rev Microbiol. 2013;67:313-36
pubmed: 24024634
Biol Lett. 2018 Nov 14;14(11):
pubmed: 30429242
Microbiol Spectr. 2013 Oct;1(1):
pubmed: 26184815
J Bacteriol. 1969 May;98(2):519-27
pubmed: 4239385
BMC Evol Biol. 2007 Nov 29;7:238
pubmed: 18047670
Nat Microbiol. 2022 Jul;7(7):1075-1086
pubmed: 35760840
Front Vet Sci. 2021 Jun 10;8:683853
pubmed: 34179174
J Bacteriol. 2007 Jun;189(11):4275-89
pubmed: 17384184
Evol Lett. 2021 Jul 15;5(5):472-483
pubmed: 34621534
Philos Trans R Soc Lond B Biol Sci. 2019 Sep 30;374(1782):20190296
pubmed: 31401961
Science. 2014 Oct 31;346(6209):630-1
pubmed: 25359973
Biochem Biophys Res Commun. 2015 Aug 28;464(3):894-900
pubmed: 26188514
Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):4979-83
pubmed: 17360396
J Biol Chem. 1970 Oct 10;245(19):5101-6
pubmed: 4248342
Nat Rev Microbiol. 2015 Nov;13(11):722-36
pubmed: 26411297
PLoS One. 2011;6(9):e24418
pubmed: 21931710
Front Microbiol. 2015 Nov 25;6:1315
pubmed: 26635776
Genome Biol. 2020 Jul 22;21(1):180
pubmed: 32698896
J Bacteriol. 1969 Nov;100(2):846-53
pubmed: 4242922
Viruses. 2022 Apr 29;14(5):
pubmed: 35632679
Science. 2015 Mar 6;347(6226):1062-4
pubmed: 25745144
Ecol Lett. 2019 Jun;22(6):987-998
pubmed: 30912262
Virology. 2004 Nov 24;329(2):425-33
pubmed: 15518820
J Virol. 1974 Aug;14(2):198-202
pubmed: 4277011
PLoS One. 2015 Mar 11;10(3):e0118557
pubmed: 25761060
Proc Natl Acad Sci U S A. 2014 Aug 5;111(31):11503-8
pubmed: 25049409
Science. 2021 Oct 22;374(6566):488-492
pubmed: 34672730
Proc Biol Sci. 2019 Jun 26;286(1905):20191110
pubmed: 31238848
Appl Environ Microbiol. 2005 Apr;71(4):1836-42
pubmed: 15812009
Annu Rev Microbiol. 2017 Sep 8;71:233-261
pubmed: 28657885
Proc Natl Acad Sci U S A. 2019 Apr 16;116(16):7911-7915
pubmed: 30926660
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Philos Trans R Soc Lond B Biol Sci. 2011 Aug 27;366(1576):2379-90
pubmed: 21768153
Appl Microbiol Biotechnol. 2021 Dec;105(24):9047-9067
pubmed: 34821965
Mol Cell. 2014 Apr 24;54(2):234-44
pubmed: 24766887
Microbiol Res. 2016 Dec;193:103-110
pubmed: 27825477
Philos Trans R Soc Lond B Biol Sci. 2013 Feb 04;368(1614):20120196
pubmed: 23382420
J Mol Evol. 2006 Jun;62(6):718-29
pubmed: 16612537
Appl Environ Microbiol. 2009 Jul;75(13):4483-90
pubmed: 19411410
Bull Hist Med. 2002 Spring;76(1):105-15
pubmed: 11875246
Nat Commun. 2022 Sep 29;13(1):5725
pubmed: 36175406
Science. 2021 Aug 27;373(6558):968-970
pubmed: 34404734