A mutation in the methionine aminopeptidase gene provides phage resistance in Streptococcus thermophilus.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
25 09 2019
25 09 2019
Historique:
received:
12
04
2019
accepted:
31
08
2019
entrez:
27
9
2019
pubmed:
27
9
2019
medline:
30
10
2020
Statut:
epublish
Résumé
Streptococcus thermophilus is a lactic acid bacterium widely used by the dairy industry for the manufacture of yogurt and specialty cheeses. It is also a Gram-positive bacterial model to study phage-host interactions. CRISPR-Cas systems are one of the most prevalent phage resistance mechanisms in S. thermophilus. Little information is available about other host factors involved in phage replication in this food-grade streptococcal species. We used the model strain S. thermophilus SMQ-301 and its virulent phage DT1, harboring the anti-CRISPR protein AcrIIA6, to show that a host gene coding for a methionine aminopeptidase (metAP) is necessary for phage DT1 to complete its lytic cycle. A single mutation in metAP provides S. thermophilus SMQ-301 with strong resistance against phage DT1. The mutation impedes a late step of the lytic cycle since phage adsorption, DNA replication, and protein expression were not affected. When the mutated strain was complemented with the wild-type version of the gene, the phage sensitivity phenotype was restored. When this mutation was introduced into other S. thermophilus strains it provided resistance against cos-type (Sfi21dt1virus genus) phages but replication of pac-type (Sfi11virus genus) phages was not affected. The mutation in the gene coding for the MetAP induces amino acid change in a catalytic domain conserved across many bacterial species. Introducing the same mutation in Streptococcus mutans also provided a phage resistance phenotype, suggesting the wide-ranging importance of the host methionine aminopeptidase in phage replication.
Identifiants
pubmed: 31554834
doi: 10.1038/s41598-019-49975-4
pii: 10.1038/s41598-019-49975-4
pmc: PMC6761271
doi:
Substances chimiques
Bacterial Proteins
0
Aminopeptidases
EC 3.4.11.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13816Commentaires et corrections
Type : ErratumIn
Références
Cobián Güemes, A. G. et al. Viruses as winners in the game of life. Annu Rev Virol 3, 197–214 (2016).
pubmed: 27741409
doi: 10.1146/annurev-virology-100114-054952
Lennon, J. T., Khatana, S. A., Marston, M. F. & Martiny, J. B. Is there a cost of virus resistance in marine cyanobacteria. ISME J 1, 300–312 (2007).
pubmed: 18043641
doi: 10.1038/ismej.2007.37
Koskella, B. & Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38, 916–931 (2014).
pubmed: 24617569
doi: 10.1111/1574-6976.12072
Avrani, S. & Lindell, D. Convergent evolution toward an improved growth rate and a reduced resistance range in Prochlorococcus strains resistant to phage. Proc Natl Acad Sci USA 112, E2191–200 (2015).
pubmed: 25922520
doi: 10.1073/pnas.1420347112
pmcid: 4418883
Vale, P. F. et al. Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus. Proc Biol Sci 282, 20151270 (2015).
pubmed: 26224708
pmcid: 4528535
Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327 (2010).
pubmed: 20348932
doi: 10.1038/nrmicro2315
Buckling, A. & Brockhurst, M. Bacteria-virus coevolution. Adv Exp Med Biol 751, 347–370 (2012).
pubmed: 22821466
doi: 10.1007/978-1-4614-3567-9_16
Samson, J. E., Magadán, A. H., Sabri, M. & Moineau, S. Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11, 675–687 (2013).
pubmed: 23979432
doi: 10.1038/nrmicro3096
Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712 (2007).
pubmed: 17379808
doi: 10.1126/science.1138140
Kronheim, S. et al. A chemical defence against phage infection. Nature 564, 283–286 (2018).
pubmed: 30518855
doi: 10.1038/s41586-018-0767-x
da Silva Duarte, V. et al. A cryptic non-inducible prophage confers phage-immunity on the Streptococcus thermophilus M17PTZA496. Viruses 11, 1 (2018).
doi: 10.3390/v11010007
Doron, S. et al. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359, 6379 (2018).
doi: 10.1126/science.aar4120
Le Marrec, C. et al. Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Appl Environ Microbiol 63, 3246–3253 (1997).
pubmed: 9251212
pmcid: 168623
doi: 10.1128/aem.63.8.3246-3253.1997
Mills, S. et al. A new phage on the ‘Mozzarella’block: bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. International dairy journal 21, 963–969 (2011).
doi: 10.1016/j.idairyj.2011.06.003
McDonnell, B. et al. Identification and analysis of a novel group of bacteriophages infecting the lactic acid bacterium Streptococcus thermophilus. Appl Environ Microbiol 82, 5153–5165 (2016).
pubmed: 27316953
pmcid: 4988201
doi: 10.1128/AEM.00835-16
McDonnell, B. et al. Global survey and genome exploration of bacteriophages infecting the lactic acid bacterium Streptococcus thermophilus. Front Microbiol 8, 1754 (2017).
pubmed: 28955321
pmcid: 5601072
doi: 10.3389/fmicb.2017.01754
Achigar, R., Magadán, A. H., Tremblay, D. M., Julia Pianzzola, M. & Moineau, S. Phage-host interactions in Streptococcus thermophilus: Genome analysis of phages isolated in Uruguay and ectopic spacer acquisition in CRISPR array. Sci Rep 7, 43438 (2017).
pubmed: 28262818
pmcid: 5338259
doi: 10.1038/srep43438
Lavelle, K. et al. A decade of Streptococcus thermophilus phage evolution in an Irish dairy plant. Appl Environ Microbiol 84, 10 (2018).
doi: 10.1128/AEM.02855-17
Lavelle, K. et al. Biodiversity of Streptococcus thermophilus phages in global dairy fermentations. Viruses 10, 577 (2018).
pmcid: 6213268
doi: 10.3390/v10100577
Ali, Y. et al. Temperate Streptococcus thermophilus phages expressing superinfection exclusion proteins of the Ltp type. Front Microbiol 5, 98 (2014).
pubmed: 24659988
pmcid: 3952083
doi: 10.3389/fmicb.2014.00098
Sun, X., Göhler, A., Heller, K. J. & Neve, H. The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. Virology 350, 146–157 (2006).
pubmed: 16643978
doi: 10.1016/j.virol.2006.03.001
Horvath, P. et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190, 1401–1412 (2008).
pubmed: 18065539
doi: 10.1128/JB.01415-07
Garneau, J. E. et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468, 67–71 (2010).
pubmed: 21048762
doi: 10.1038/nature09523
Deveau, H. et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190, 1390–1400 (2008).
pubmed: 18065545
doi: 10.1128/JB.01412-07
Hynes, A. P. et al. An anti-CRISPR from a virulent streptococcal phage inhibits Streptococcus pyogenes Cas9. Nat Microbiol 2, 1374–1380 (2017).
pubmed: 28785032
doi: 10.1038/s41564-017-0004-7
Hynes, A. P. et al. Widespread anti-CRISPR proteins in virulent bacteriophages inhibit a range of Cas9 proteins. Nat Commun 9, 2919 (2018).
pubmed: 30046034
pmcid: 6060171
doi: 10.1038/s41467-018-05092-w
McDonnell, B., Mahony, J., Hanemaaijer, L., Kouwen, T. R. H. M. & van Sinderen, D. Generation of bacteriophage-insensitive mutants of Streptococcus thermophilus via an antisense RNA CRISPR-Cas silencing approach. Appl Environ Microbiol 84, 4 (2018).
doi: 10.1128/AEM.01733-17
Szymczak, P. et al. Cell wall glycans mediate recognition of the dairy bacterium Streptococcus thermophilus by bacteriophages. Appl Environ Microbiol 84, 23 (2018).
doi: 10.1128/AEM.01847-18
Tremblay, D. M. & Moineau, S. Complete genomic sequence of the lytic bacteriophage DT1 of Streptococcus thermophilus. Virology 255, 63–76 (1999).
pubmed: 10049822
doi: 10.1006/viro.1998.9525
Magadán, A. H., Dupuis, M. È., Villion, M. & Moineau, S. Cleavage of phage DNA by the Streptococcus thermophilus CRISPR3-Cas system. PLoS One 7,, e40913 (2012).
doi: 10.1371/journal.pone.0040913
De Vos, W. M. Gene cloning and expression in lactic streptococci. FEMS Microbiology Letters 46, 281–295 (1987).
doi: 10.1111/j.1574-6968.1987.tb02466.x
Hynes, A. P. et al. Detecting natural adaptation of the Streptococcus thermophilus CRISPR-Cas systems in research and classroom settings. Nat Protoc 12, 547–565 (2017).
pubmed: 28207002
doi: 10.1038/nprot.2016.186
Garvey, P., Hill, C. & Fitzgerald, G. F. The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Appl Environ Microbiol 62, 676–679 (1996).
pubmed: 16535245
pmcid: 1388783
doi: 10.1128/aem.62.2.676-679.1996
Boucher, I., Emond, E., Dion, E., Montpetit, D. & Moineau, S. Microbiological and molecular impacts of AbiK on the lytic cycle of Lactococcus lactis phages of the 936 and P335 species. Microbiology 146, 445–453 (2000).
pubmed: 10708383
doi: 10.1099/00221287-146-2-445
Bissonnette, F., Labrie, S., Deveau, H., Lamoureux, M. & Moineau, S. Characterization of mesophilic mixed starter cultures used for the manufacture of aged cheddar cheese. J Dairy Sci 83, 620–627 (2000).
pubmed: 10791775
doi: 10.3168/jds.S0022-0302(00)74921-6
Labrie, S. J. et al. Complete genome sequence of Streptococcus thermophilus SMQ-301, a model strain for phage-host interactions. Genome Announc 3, 3 (2015).
doi: 10.1128/genomeA.00480-15
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6, 343–345 (2009).
pubmed: 19363495
doi: 10.1038/nmeth.1318
Scaltriti, E. et al. Structure and function of phage p2 ORF34(p2), a new type of single-stranded DNA binding protein. Mol Microbiol 73, 1156-1170 (2009).
Gardan, R., Besset, C., Guillot, A., Gitton, C. & Monnet, V. The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. J Bacteriol 191, 4647–4655 (2009).
pubmed: 19447907
pmcid: 2704715
doi: 10.1128/JB.00257-09
Fontaine, L. et al. Development of a versatile procedure based on natural transformation for marker-free targeted genetic modification in Streptococcus thermophilus. Appl Environ Microbiol 76, 7870–7877 (2010).
pubmed: 20935129
pmcid: 2988589
doi: 10.1128/AEM.01671-10
Dufour, D., Cordova, M., Cvitkovitch, D. G. & Lévesque, C. M. Regulation of the competence pathway as a novel role associated with a streptococcal bacteriocin. J Bacteriol 193, 6552–6559 (2011).
pubmed: 21984782
pmcid: 3232909
doi: 10.1128/JB.05968-11
Delisle, A. L. et al. Biology and genome sequence of Streptococcus mutans phage M102AD. Appl Environ Microbiol 78, 2264–2271 (2012).
pubmed: 22287009
pmcid: 3302630
doi: 10.1128/AEM.07726-11
Arya, T., Kishor, C., Saddanapu, V., Reddi, R. & Addlagatta, A. Discovery of a new genetic variant of methionine aminopeptidase from Streptococci with possible post-translational modifications: biochemical and structural characterization. PLoS One 8, e75207 (2013).
pubmed: 24124477
pmcid: 3790777
doi: 10.1371/journal.pone.0075207
Lowther, W. T. et al. Escherichia coli methionine aminopeptidase: implications of crystallographic analyses of the native, mutant, and inhibited enzymes for the mechanism of catalysis. Biochemistry 38, 7678–7688 (1999).
pubmed: 10387007
doi: 10.1021/bi990684r
Copik, A. J. et al. Kinetic and spectroscopic characterization of the H178A methionyl aminopeptidase from Escherichia coli. Biochemistry 42, 6283–6292 (2003).
pubmed: 12755633
doi: 10.1021/bi027327s
Duplessis, M. & Moineau, S. Identification of a genetic determinant responsible for host specificity in Streptococcus thermophilus bacteriophages. Molecular microbiology 41, 325–336 (2001).
pubmed: 11489121
doi: 10.1046/j.1365-2958.2001.02521.x
Lévesque, C. et al. Genomic organization and molecular analysis of virulent bacteriophage 2972 infecting an exopolysaccharide-producing Streptococcus thermophilus strain. Appl Environ Microbiol 71, 4057–4068 (2005).
pubmed: 16000821
pmcid: 1169050
doi: 10.1128/AEM.71.7.4057-4068.2005
Hirel, P.-H., Schmitter, M. J., Dessen, P., Fayat, G. & Blanquet, S. Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc Natl Acad Sci 86, 8247–8251 (1989).
pubmed: 2682640
doi: 10.1073/pnas.86.21.8247
pmcid: 298257
Xiao, Q., Zhang, F., Nacev, B. A., Liu, J. O. & Pei, D. Protein N-terminal processing: substrate specificity of Escherichia coli and human methionine aminopeptidases. Biochemistry 49, 5588–5599 (2010).
pubmed: 20521764
doi: 10.1021/bi1005464
Giglione, C., Boularot, A. & Meinnel, T. Protein N-terminal methionine excision. Cell Mol Life Sci 61, 1455–1474 (2004).
pubmed: 15197470
doi: 10.1007/s00018-004-3466-8
Giglione, C., Fieulaine, S. & Meinnel, T. N-terminal protein modifications: Bringing back into play the ribosome. Biochimie 114, 134–146 (2015).
pubmed: 25450248
doi: 10.1016/j.biochi.2014.11.008
Chang, S. Y., McGary, E. C. & Chang, S. Methionine aminopeptidase gene of Escherichia coli is essential for cell growth. J Bacteriol 171, 4071–4072 (1989).
pubmed: 2544569
pmcid: 210164
doi: 10.1128/jb.171.7.4071-4072.1989
Miller, C. G., Kukral, A. M., Miller, J. L. & Movva, N. R. pepM is an essential gene in Salmonella typhimurium. J Bacteriol 171, 5215–5217 (1989).
pubmed: 2670909
pmcid: 210346
doi: 10.1128/jb.171.9.5215-5217.1989
Zuo, S., Guo, Q., Ling, C. & Chang, Y. H. Evidence that two zinc fingers in the methionine aminopeptidase from Saccharomyces cerevisiae are important for normal growth. Mol Gen Genet 246, 247–253 (1995).
pubmed: 7862096
doi: 10.1007/BF00294688