The plasmid complement of Lactococcus lactis UC509.9 encodes multiple bacteriophage resistance systems

Applied and Environmental Microbiology

Volumn 80, Issue 14, 2014, Pages 4341-4349

  Ainsworth, Stuart ^a   Mahony, Jennifer ^a   van Sinderen, Douwe ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; ENCODING (SYMBOLS); STRAIN;

CAPSID PROTEINS; FERMENTED DAIRY PRODUCTS; LACTIS STRAIN; LACTOCOCCUS LACTIS; LACTOCOCCUS LACTIS SUBSP. CREMORIS; PHENOTYPIC TRAITS; PLANT ORIGIN; STARTER CULTURES;

DNA;

ADAPTATION; BACTERIOPHAGE; BACTERIUM; FERMENTATION; MUTATION; PHENOTYPE; PLASMID;

BACTERIAL DNA;

BACTERIAL CHROMOSOME; BACTERIOPHAGE; BIOLOGY; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOCOCCUS LACTIS; MOLECULAR CLONING; PHENOTYPE; PLASMID; VIROLOGY;

BACTERIOPHAGES; CHROMOSOMES, BACTERIAL; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; LACTOCOCCUS LACTIS; PHENOTYPE; PLASMIDS;

EID: 84903170936     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01070-14     Document Type: Article

References (66)

1. de Vos WM. 2011. Systems solutions by lactic acid bacteria: from paradigms to practice. Microb. Cell Fact. 10(Suppl 1):S2. http://dx.doi.org/10.1186/1475-2859-10-S1-S2.
2. Bachmann H, Starrenburg MJ, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE. 2012. Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution. Genome Res. 22:115-124. http://dx.doi.org/10.1101/gr.121285.111.
3. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O'Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D. 2006. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. USA. 103:15611-15616. http: //dx.doi.org/10.1073/pnas.0607117103.
4. Ainsworth S, Zomer A, de Jager V, Bottacini F, van Hijum SA, Mahony J, van Sinderen D. 2013. Complete genome of Lactococcus lactis subsp. cremoris UC509.9, host for a model lactococcal P335 bacteriophage. Genome Announc. 1(1):e00119-12. http://dx.doi.org/10.1128/genomeA.00036-12.
5. Kelly WJ, Ward LJ, Leahy SC. 2010. Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol. Evol. 2:729-744. http://dx.doi.org/10.1093/gbe/evq056.
6. Klijn N, Weerkamp AH, de Vos WM. 1995. Detection and characterization of lactose-utilizing Lactococcus spp. in natural ecosystems. Appl. Environ. Microbiol. 61:788-792.
7. Salama MS, Musafija-Jeknic T, Sandine WE, Giovannoni SJ. 1995. An ecological study of lactic acid bacteria: isolation of new strains of Lactococcus including Lactococcus lactis subspecies cremoris. J. Dairy Sci. 78: 1004-1017. http://dx.doi.org/10.3168/jds.S0022-0302(95)76716-9.
8. Mills S, McAuliffe OE, Coffey A, Fitzgerald GF, Ross RP. 2006. Plasmids of lactococci: genetic accessories or genetic necessities? FEMS Microbiol. Rev. 30:243-273. http://dx.doi.org/10.1111/j.1574-6976.2005.00011.x.
9. Efstathiou JD, McKay LL. 1977. Inorganic salts resistance associated with a lactose-fermenting plasmid in Streptococcus lactis. J. Bacteriol. 130:257-265.
10. Siezen RJ, Renckens B, van Swam I, Peters S, van Kranenburg R, Kleerebezem M, de Vos WM. 2005. Complete sequences of four plasmids of Lactococcus lactis subsp. cremoris SK11 reveal extensive adaptation to the dairy environment. Appl. Environ. Microbiol. 71:8371-8382. http: //dx.doi.org/10.1128/AEM.71.12.8371-8382.2005.
11. Fallico V, Ross RP, Fitzgerald GF, McAuliffe O. 2012. Novel conjugative plasmids from the natural isolate Lactococcus lactis subspecies cremoris DPC3758: a repository of genes for the potential improvement of dairy starters. J. Dairy. Sci. 95:3593-3608. http://dx.doi.org/10.3168/jds.2011-5255.
12. Bolotin A, Quinquis B, Ehrlich SD, Sorokin A. 2012. Complete genome sequence of Lactococcus lactis subsp. cremoris A76. J. Bacteriol. 194:1241-1242. http://dx.doi.org/10.1128/JB.06629-11.
13. Gorecki RK, Koryszewska-Baginska A, Golebiewski M, Zylinska J, Grynberg M, Bardowski JK. 2011. Adaptative potential of the Lactococcus lactis IL594 strain encoded in its 7 plasmids. PLoS One 6(7):e22238. http: //dx.doi.org/10.1371/journal.pone.0022238.
14. Mahony J, Murphy J, van Sinderen D. 2012. Lactococcal 936-type phages and dairy fermentation problems: from detection to evolution and prevention. Front. Microbiol. 3:335. http://dx.doi.org/10.3389/fmicb.2012.00335.
15. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317-327. http://dx.doi.org/10.1038/nrmicro2315.
16. Chopin MC, Chopin A, Bidnenko E. 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473-479. http: //dx.doi.org/10.1016/j.mib.2005.06.006.
17. Millen AM, Horvath P, Boyaval P, Romero DA. 2012. Mobile CRISPR/Cas-mediated bacteriophage resistance in Lactococcus lactis. PLoS One 7:e51663. http://dx.doi.org/10.1371/journal.pone.0051663.
18. Klaenhammer TR, Sanozky RB. 1985. Conjugal transfer from Streptococcus lactis ME2 of plasmids encoding phage resistance, nisin resistance and lactose-fermenting ability: evidence for a high-frequency conjugative plasmid responsible for abortive infection of virulent bacteriophage. J. Gen. Microbiol. 131:1531-1541.
19. Hill C, Miller LA, Klaenhammer TR. 1990. Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci. Appl. Environ. Microbiol. 56:2255-2258.
20. O'Connor L, Tangney M, Fitzgerald GF. 1999. Expression, regulation, and mode of action of the AbiG abortive infection system of Lactococcus lactis subsp. cremoris UC653. Appl. Environ. Microbiol. 65:330-335.
21. Bidnenko E, Chopin A, Ehrlich SD, Chopin MC. 2009. Activation of mRNA translation by phage protein and low temperature: the case of Lactococcus lactis abortive infection system AbiD1. BMC Mol. Biol. 10:4. http://dx.doi.org/10.1186/1471-2199-10-4.
22. Samson JE, Belanger M, Moineau S. 2013. Effect of the abortive infection mechanism and type III toxin/antitoxin system AbiQ on the lytic cycle of Lactococcus lactis phages. J. Bacteriol. 195:3947. http://dx.doi.org/10.1128 /JB.00296-13.
23. Labrie SJ, Tremblay DM, Moisan M, Villion M, Magadan AH, Campanacci V, Cambillau C, Moineau S. 2012. Involvement of the major capsid protein and two early-expressed phage genes in the activity of the lactococcal abortive infection mechanism AbiT. Appl. Environ. Microbiol. 78:6890-6899. http://dx.doi.org/10.1128/AEM.01755-12.
24. Haaber J, Samson JE, Labrie SJ, Campanacci V, Cambillau C, Moineau S, Hammer K. 2010. Lactococcal abortive infection protein AbiV interacts directly with the phage protein SaV and prevents translation of phage proteins. Appl. Environ. Microbiol. 76:7085-7092. http://dx.doi.org/10.1128/AEM.00093-10.
25. Costello V. 1988. Characterization of bacteriophage-host interactions in Streptococcus cremoris UC503 and related lactic streptococci. Ph.D. thesis. National University of Ireland, University College Cork, Cork, Ireland.
26. Seegers JFML, Mc Grath S, O'Connell-Motherway M, Arendt EK, van de Guchte M, Creaven M, Fitzgerald GF, van Sinderen D. 2004. Molecular and transcriptional analysis of the temperate lactococcal bacteriophage Tuc2009. Virology 329:40-52. http://dx.doi.org/10.1016/j.virol.2004.07.003.
27. Collins B, Bebeacua C, Mahony J, Blangy S, Douillard F, Veesler D, Cambillau C, van Sinderen D. 2013. Structure and functional analysis of the host recognition device of lactococcal phage Tuc2009. J. Virol. 87: 8429-8440. http://dx.doi.org/10.1128/JVI.00907-13.
28. Stockdale SR, Mahony J, Courtin P, Chapot-Chartier MP, van Pijkeren JP, Britton RA, Neve H, Heller KJ, Aideh B, Vogensen FK, van Sinderen D. 2013. The lactococcal phages Tuc2009 and TP901-1 incorporate two alternate forms of their tail fibre into their virions for infection specialization. J. Biol. Chem. 288:5581-5590. http://dx.doi.org/10.1074/jbc.M112.444901.
29. Kuipers OP, de Ruyter PGGA, Kleerebezem M, de Vos WM. 1998. Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64:15-21. http://dx.doi.org/10.1016/S0168-1656(98)00100-X.
30. Mahony J, McGrath S, Fitzgerald GF, van Sinderen D. 2008. Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl. Environ. Microbiol. 74:6206-6215. http://dx.doi.org/10.1128/AEM.01053-08.
31. Lillehaug D. 1997. An improved plaque assay for poor plaque-producing temperate lactococcal bacteriophages. J. Appl. Microbiol. 83:85-90. http: //dx.doi.org/10.1046/j.1365-2672.1997.00193.x.
32. Burgess C, O'Connell-Motherway M, Sybesma W, Hugenholtz J, van Sinderen D. 2004. Riboflavin production in Lactococcus lactis: potential for in situ production of vitamin-enriched foods. Appl. Environ. Microbiol. 70:5769-5777. http://dx.doi.org/10.1128/AEM.70.10.5769-5777.2004.
33. O'Driscoll J, Glynn F, Cahalane O, O'Connell-Motherway M, Fitzgerald GF, Van Sinderen D. 2004. Lactococcal plasmid pNP40 encodes a novel, temperature-sensitive restriction-modification system. Appl. Environ. Microbiol. 70:5546-5556. http://dx.doi.org/10.1128/AEM.70.9.5546-5556.2004.
34. Gasson MJ. 1983. Plasmid complements of Streptococcus lactisNCDO712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 154:1-9.
35. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 8:119. http://dx.doi.org/10.1186 /1471-2105-11-119.
36. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http: //dx.doi.org/10.1093/nar/25.17.3389.
37. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945. http://dx.doi.org/10.1093/bioinformatics/16.10.944.
38. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. 2010. The Pfam protein families database. Nucleic Acids Res. 38:D211-D222. http://dx.doi.org/10.1093/nar/gkp985.
39. Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28:27-30. http://dx.doi.org/10.1093/nar/28.1.27.
40. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. http://dx.doi.org/10.1186/1471-2105-4-41.
41. Seegers JF, van Sinderen D, Fitzgerald GF. 2000. Molecular characterization of the lactococcal plasmid pCIS3: natural stacking of specificity subunits of a type I restriction/modification system in a single lactococcal strain. Microbiology 146:435-443. http://mic.sgmjournals.org/content/1 46/2/435.long.
42. Kiewiet R, Bron S, de Jonge K, Venema G, Seegers JF. 1993. Theta replication of the lactococcal plasmid pWVO2. Mol. Microbiol. 10:319-327. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01958.x.
43. McKay LL, Baldwin KA. 1974. Simultaneous loss of proteinase-and lactose-utilizing enzyme activities in Streptococcus lactis and reversal of loss by transduction. Appl. Microbiol. 28:342-346.
44. Yu W, Gillies K, Kondo JK, Broadbent JR, McKay LL. 1996. Loss of plasmid-mediated oligopeptide transport system in lactococci: another reason for slow milk coagulation. Plasmid 35:145-155. http://dx.doi.org /10.1006/plas.1996.0017.
45. Yu W, Gillies K, Kondo JK, Broadbent JR, McKay LL. 1995. Plasmidmediated oligopeptide transport system in lactococci. Dev. Biol. Stand. 85:509-521.
46. Savijoki K, Ingmer H, Varmanen P. 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biot. 71:394-406. http://dx.doi.org/10.1007/s00253-006-0427-1.
47. Steele J, Broadbent J, Kok J. 2013. Perspectives on the contribution of lactic acid bacteria to cheese flavor development. Curr. Opin. Biotechnol. 24:135-141. http://dx.doi.org/10.1016/j.copbio.2012.12.001.
48. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788. http://dx.doi.org/10.1038/nrmicro1273.
49. Stoddard GW, Petzel JP, Vanbelkum MJ, Kok J, Mckay LL. 1992. Molecular analyses of the lactococcin A gene-cluster from Lactococcus lactis subsp. lactis biovar. diacetylactis Wm4. Appl. Environ. Microbiol. 58: 1952-1961.
50. Johnsen L, Dalhus B, Leiros I, Nissen-Meyer J. 2005. 1.6-Å crystal structure of EntA-im. A bacterial immunity protein conferring immunity to the antimicrobial activity of the pediocin-like bacteriocin enterocin A. J. Biol. Chem. 280:19045-19050. http://dx.doi.org/10.1074/jbc.M501386200.
51. Mahony J, Kot W, Murphy J, Ainsworth S, Neve H, Hansen LH, Heller KJ, Sørensen SJ, Hammer K, Cambillau C, Vogensen FK, van Sinderen D. 2013. Investigation of the relationship between lactococcal host cell wall polysaccharide genotype and 936 phage receptor binding protein phylogeny. Appl. Environ. Microbiol. 79:4385-4392. http://dx.doi.org/10.1128/AEM.00653-13.
52. Davis R, van der Lelie D, Mercenier A, Daly C, Fitzgerald GF. 1993. ScrFI restriction-modification system of Lactococcus lactis subsp. cremoris UC503: cloning and characterization of two ScrFI methylase genes. Appl. Environ. Microbiol. 59:777-785.
53. O'Sullivan D, Twomey DP, Coffey A, Hill C, Fitzgerald GF, Ross RP. 2000. Novel type I restriction specificities through domain shuffling of HsdS subunits in Lactococcus lactis. Mol. Microbiol. 36:866-875. http://dx.doi.org/10.1046/j.1365-2958.2000.01901.x.
54. Schouler C, Gautier M, Ehrlich SD, Chopin MC. 1998. Combinational variation of restriction modification specificities in Lactococcus lactis. Mol. Microbiol. 28:169-178.
55. Parreira R, Ehrlich SD, Chopin MC. 1996. Dramatic decay of phage transcripts in lactococcal cells carrying the abortive infection determinant AbiB. Mol. Microbiol. 19:221-230. http://dx.doi.org/10.1046/j.1365-2958.1996.371896.x.
56. Anba J, Bidnenko E, Hillier A, Ehrlich D, Chopin MC. 1995. Characterization of the lactococcal abiD1 gene coding for phage abortive infection. J. Bacteriol. 177:3818-3823.
57. Cluzel PJ, Chopin A, Ehrlich SD, Chopin MC. 1991. Phage abortive infection mechanism from Lactococcus lactis subsp. lactis, expression of which is mediated by an Iso-ISS1 element. Appl. Environ. Microbiol. 57: 3547-3551.
58. Dunn N, Gunsalus I. 1973. Transmissible plasmid coding early enzymes of naphthalene oxidation in Pseudomonas putida. J. Bacteriol. 114:974-979.
59. Deveau H, Labrie SJ, Chopin MC, Moineau S. 2006. Biodiversity and classification of lactococcal phages. Appl. Environ. Microbiol. 72:4338-4346. http://dx.doi.org/10.1128/AEM.02517-05.
60. Parreira R. 1996. Characterization of the abiB-encoded phage abortive infection mechanism of Lactococcus lactis subsp. lactis. Ph.D. dissertation. Université de Paris XI, Paris, France.
61. Chandry PS, Moore SC, Boyce JD, Davidson BE, Hillier AJ. 1997. Analysis of the DNA sequence, gene expression, origin of replication and modular structure of the Lactococcus lactis lytic bacteriophage sk1. Mol. Microbiol. 26:49-64. http://dx.doi.org/10.1046/j.1365-2958.1997.5491926.x.
62. Snyder L. 1995. Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents? Mol. Microbiol. 15:415-420. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02255.x.
63. McGrath S, Seegers JF, Fitzgerald GF, van Sinderen D. 1999. Molecular characterization of a phage-encoded resistance system in Lactococcus lactis. Appl. Environ. Microbiol. 65:1891-1899.
64. Jarvis AW. 1984. Differentiation of lactic streptococcal phages into phage species by DNA-DNA homology. Appl. Environ. Microbiol. 47:343-349.
65. Lubbers MW, Waterfield NR, Beresford TP, Le Page RW, Jarvis AW. 1995. Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes. Appl. Environ. Microbiol. 61:4348-4356.
66. Mahony J, Deveau H, Mc Grath S, Ventura M, Canchaya C, Moineau S, Fitzgerald GF, van Sinderen D. 2006. Sequence and comparative genomic analysis of lactococcal bacteriophages jj50, 712 and P008: evolutionary insights into the 936 phage species. FEMS Microbiol. Lett. 261: 253-261. http://dx.doi.org/10.1111/j.1574-6968.2006.00372.x.