Bacteriocins of non-aureus staphylococci isolated from bovine milk

Applied and Environmental Microbiology

Volumn 83, Issue 17, 2017, Pages

  Carson, Domonique A ^a   Barkema, Herman W ^a   Naushad, Sohail ^a   De Buck, Jeroen ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bacteriocins; Cattle; Coagulasenegative staphylococci; Mastitis; Staphylococcus; Staphylococcus aureus

Indexed keywords

BACTERIAL PROTEIN; BACTERIOCIN;

ANIMAL; BACTERIAL GENOME; BIOSYNTHESIS; BOVINE; CLASSIFICATION; FEMALE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MILK; MULTIGENE FAMILY; STAPHYLOCOCCUS;

ANIMALS; BACTERIAL PROTEINS; BACTERIOCINS; CATTLE; FEMALE; GENOME, BACTERIAL; MILK; MULTIGENE FAMILY; STAPHYLOCOCCUS;

EID: 85027461947     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01015-17     Document Type: Article

References (66)

1. Piepers S, De Meulemeester L, de Kruif A, Opsomer G, Barkema HW, De Vliegher S. 2007. Prevalence and distribution of mastitis pathogens in subclinically infected dairy cows in Flanders, Belgium. J Dairy Res 74: 478-483. https://doi.org/10.1017/S0022029907002841.
2. Pitkälä A, Haveri M, Pyörälä S, Myllys V, Honkanen-Buzalski T. 2004. Bovine mastitis in Finland 2001-prevalence, distribution of bacteria, and antimicrobial resistance. J Dairy Sci 87:2433-2441. https://doi.org/10.3168/jds.S0022-0302(04)73366-4.
3. Sampimon OC, Barkema HW, Berends IMGA, Sol J, Lam TJGM. 2009. Prevalence and herd-level risk factors for intramammary infection with coagulase-negative staphylococci in Dutch dairy herds. Vet Microbiol 134:37-44. https://doi.org/10.1016/j.vetmic.2008.09.010.
4. White DG, Harmon RJ, Matos JES, Langlois BE. 1989. Isolation and identification of coagulase-negative Staphylococcus species from bovine body sites and streak canals of nulliparous heifers. J Dairy Sci 72: 1886-1892. https://doi.org/10.3168/jds.S0022-0302(89)79307-3.
5. De Vliegher S, Opsomer G, Vanrolleghem A, Devriese LA, Sampimon OC, Sol J, Barkema HW, Haesebrouck F, de Kruif A. 2004. In vitro growth inhibition of major mastitis pathogens by Staphylococcus chromogenes originating from teat apices of dairy heifers. Vet Microbiol 101:215-221. https://doi.org/10.1016/j.vetmic.2004.03.020.
6. Matthews KR, Harmon RJ, Smith BA. 1990. Protective effect of Staphylococcus chromogenes infection against Staphylococcus aureus infection in the lactating bovine mammary gland. J Dairy Sci 73:3457-3462. https://doi.org/10.3168/jds.S0022-0302(90)79044-3.
7. dos Santos Nascimento J, Fagundes PC, Brito MAVP, Santos KRN, Bastos MCF. 2005. Production of bacteriocins by coagulase-negative staphylococci involved in bovine mastitis. Vet Microbiol 106:61-71. https://doi.org/10.1016/j.vetmic.2004.10.014.
8. Braem G, Stijlemans B, Van Haken W, De Vliegher S, De Vuyst L, Leroy F. 2014 Antibacterial activities of coagulase-negative staphylococci from bovine teat apex skin and their inhibitory effect on mastitis-related pathogens. J Appl Microbiol 116:1084-1093. https://doi.org/10.1111/jam.12447.
9. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777-788. https://doi.org/10.1038/nrmicro1273.
10. Cotter PD, Ross RP, Hill C. 2013. Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11:95-105. https://doi.org/10.1038/nrmicro2937.
11. Sears PM, Smith BS, Stewart WK, Gonzalez RN, Rubino SD, Gusik SA, Kulisek ES, Projan SJ, Blackburn P. 1992. Evaluation of a nisin-based germicidal formulation on teat skin of live cows. J Dairy Sci 75: 3185-3190. https://doi.org/10.3168/jds.S0022-0302(92)78083-7.
12. Crispie F, Twomey D, Flynn J, Hill C, Ross P, Meaney W. 2005. The lantibiotic lacticin 3147 produced in a milk-based medium improves the efficacy of a bismuth-based teat seal in cattle deliberately infected with Staphylococcus aureus. J Dairy Res 72:159-167. https://doi.org/10.1017/S0022029905000816.
13. Marsh AJ, O'Sullivan O, Ross RP, Cotter PD, Hill C. 2010. In silico analysis highlights the frequency and diversity of type 1 lantibiotic gene clusters in genome sequenced bacteria. BMC Genomics 11:679-700. https://doi.org/10.1186/1471-2164-11-679.
14. Begley M, Cotter PD, Hill C, Ross RP. 2009. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 75:5451-5460. https://doi.org/10.1128/AEM.00730-09.
15. Kjos M, Borrero J, Opsata M, Birri DJ, Holo H, Cintas LM, Snipen L, Hernández PE, Nes IF, Diep DB. 2011. Target recognition, resistance, immunity and genome mining of class II bacteriocins from Grampositive bacteria. Microbiology 157:3256-3267. https://doi.org/10.1099/mic.0.052571-0.
16. Wang H, Fewer DP, Sivonen K. 2011. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS One 6:e22384. https://doi.org/10.1371/journal.pone.0022384.
17. Singh M, Sareen D. 2014. Novel LanT associated lantibiotic clusters identified by genome database mining. PLoS One 9:e91352. https://doi.org/10.1371/journal.pone.0091352.
18. Azevedo AC, Bento CBP, Ruiz JC, Queiroz MV, Mantovani HC. 2015. Distribution and genetic diversity of bacteriocin gene clusters in rumen microbial genomes. Appl Environ Microbiol 81:7290-7304. https://doi.org/10.1128/AEM.01223-15.
19. Letzel A-C, Pidot SJ, Hertweck C. 2014. Genome mining for ribosomally synthesized and post-translationally modified peptides (RiPPs) in anaerobic bacteria. BMC Genomics 15:983. https://doi.org/10.1186/1471-2164-15-983.
20. Singh NP, Tiwari A, Bansal A, Thakur S, Sharma G, Gabrani R. 2015. Genome level analysis of bacteriocins of lactic acid bacteria. Comput Biol Chem 56:1-6. https://doi.org/10.1016/j.compbiolchem.2015.02.013.
21. Walsh CJ, Guinane CM, Hill C, Ross RP, O'Toole PW, Cotter PD. 2015. In silico identification of bacteriocin gene clusters in the gastrointestinal tract, based on the Human Microbiome Project's reference genome database. BMC Microbiol 15:183. https://doi.org/10.1186/s12866-015-0515-4.
22. Naushad S, Barkema H, Luby C, Condas L, Nobrega D, Carson D, De Buck J. 2016. Comprehensive phylogenetic analysis of bovine non-aureus staphylococci species based on whole-genome sequencing. Front Microbiol 7:1990. https://doi.org/10.3389/fmicb.2016.01990.
23. Iwatsuki M, Tomoda H, Uchida R, Gouda H, Hirono S, Omura S. 2006. Lariatins, antimycobacterial peptides produced by rhodococcus sp. K01-B0171, have a lasso structure. J Am Chem Soc 128:7486-7491. https://doi.org/10.1021/ja056780z.
24. Bierbaum G, Götz F, Peschel A, Kupke T, van de Kamp M, Sahl HG. 1996. The biosynthesis of the lantibiotics epidermin, gallidermin, Pep5 and epilancin K7. Antonie Van Leeuwenhoek 69:119-127. https://doi.org/10.1007/BF00399417.
25. Asaduzzaman SM, Sonomoto K. 2009. Lantibiotics: diverse activities and unique modes of action. J Biosci Bioeng 107:475-487. https://doi.org/10.1016/j.jbiosc.2009.01.003.
26. Knerr PJ, van der Donk WA. 2012. Discovery, biosynthesis, and engineering of lantipeptides. Annu Rev Biochem 81:479-505. https://doi.org/10.1146/annurev-biochem-060110-113521.
27. Bastos MCF, Ceotto H, Coelho MLV, Nascimento JS. 2009. Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications. Curr Pharm Biotechnol 10:38-61. https://doi.org/10.2174/138920109787048580.
28. Nascimento JS, Ceotto H, Nascimento SB, Giambiagi-deMarval M, Santos KRN, Bastos MCF. 2006. Bacteriocins as alternative agents for control of multiresistant staphylococcal strains. Lett Appl Microbiol 42:215-221. https://doi.org/10.1111/j.1472-765X.2005.01832.x.
29. Varella Coelho ML, Nascimento JS, Fagundes PC, Madureira DJ, Oliveira SS, Vasconcelos Paiva Brito MA, Freire Bastos MDC. 2007. Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158: 625-630. https://doi.org/10.1016/j.resmic.2007.07.002.
30. Lubelski J, Rink R, Khusainov R, Moll GN, Kuipers OP. 2008. Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci 65:455-476. https://doi.org/10.1007/s00018-007-7171-2.
31. Sashihara T, Toshihiro S, Hirokazu K, Toshimasa H, Asaho A. 2000. A novel lantibiotic, Nukacin ISK-1, of Staphylococcus warneri ISK-1. Biosci Biotechnol Biochem 64:2420. https://doi.org/10.1271/bbb.64.2420.
32. Ceotto H, Holo H, da Costa KFS, Nascimento JS, Salehian Z, Nes IF, Bastos MDC. 2010. Nukacin 3299, a lantibiotic produced by Staphylococcus simulans 3299 identical to nukacin ISK-1. Vet Microbiol 146:124-131. https://doi.org/10.1016/j.vetmic.2010.04.032.
33. Dischinger J, Josten M, Szekat C, Sahl H-G, Bierbaum G. 2009. Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13. PLoS One 4:e6788. https://doi.org/10.1371/journal.pone.0006788.
34. McClerren AL, Cooper LE, Quan C, Thomas PM, Kelleher NL, van der Donk WA. 2006. Discovery and in vitro biosynthesis of haloduracin, a twocomponent lantibiotic. Proc Natl Acad Sci U S A 103:17243-17248. https://doi.org/10.1073/pnas.0606088103.
35. Fluhe L, Marahiel MA. 2013. Radical S-adenosylmethionine enzyme catalyzed thioether bond formation in sactipeptide biosynthesis. Curr Opin Chem Biol 17:605-612. https://doi.org/10.1016/j.cbpa.2013.06.031.
36. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, Cotter PD, Craik DJ, Dawson M, Dittmann E, Donadio S, Dorrestein PC, Entian K-D, Fischbach MA, Garavelli JS, Göransson U, Gruber CW, Haft DH, Hemscheidt TK, Hertweck C, Hill C, Horswill AR, Jaspars M, Kelly WL, Klinman JP, Kuipers OP, Link AJ, Liu W, Marahiel MA, Mitchell DA, Moll GN, Moore BS, Müller R, Nair SK, Nes IF, Norris GE, Olivera BM, Onaka H, Patchett ML, Piel J, Reaney MJT, Rebuffat S, Ross RP, Sahl H-G, Schmidt EW, Selsted ME, et al. 2013 Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30:108-160. https://doi.org/10.1039/C2NP20085F.
37. Murphy K, O'Sullivan O, Rea MC, Cotter PD, Ross RP, Hill C. 2011. Genome mining for radical SAM protein determinants reveals multiple sactibioticlike gene clusters. PLoS One 6:e20852. https://doi.org/10.1371/journal.pone.0020852.
38. Shelburne CE, An FY, Dholpe V, Ramamoorthy A, Lopatin DE, Lantz MS. 2007 The spectrum of antimicrobial activity of the bacteriocin subtilosin A. J Antimicrob Chemother 59:297-300. https://doi.org/10.1093/jac/dkl495.
39. Maksimov MO, Link AJ. 2014. Prospecting genomes for lasso peptides. J Ind Microbiol Biotechnol 41:333-344. https://doi.org/10.1007/s10295-013-1357-4.
40. Hegemann JD, Zimmermann M, Xie X, Marahiel MA. 2015. Lasso peptides: an intriguing class of bacterial natural products. Acc Chem Res 48:1909-1919. https://doi.org/10.1021/acs.accounts.5b00156.
41. Potter A, Ceotto H, Coelho MLV, Guimarães AJ, Bastos MDC. 2014. The gene cluster of aureocyclicin 4185: the first cyclic bacteriocin of Staphylococcus aureus. Microbiology 160:917-928. https://doi.org/10.1099/mic.0.075689-0.
42. Martínez B, Fernández Ma Suárez JE, Rodríguez A. 1999. Synthesis of lactococcin 972, a bacteriocin produced by Lactococcus lactis IPLA 972, depends on the expression of a plasmid-encoded bicistronic operon. Microbiology 145:3155-3161. https://doi.org/10.1099/00221287-145-11-3155.
43. Kjos M, Nes IF, Diep DB. 2009. Class II one-peptide bacteriocins target a phylogenetically defined subgroup of mannose phosphotransferase systems on sensitive cells. Microbiology 155:2949. https://doi.org/10.1099/mic.0.030015-0.
44. Nascimento JS, Abrantes J, Giambiagi-deMarval M, Bastos MCF. 2004. Growth conditions required for bacteriocin production by strains of Staphylococcus aureus. World J Microbiol Biotechnol 20:941-947. https://doi.org/10.1007/s11274-004-3626-x.
45. Leroy F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67-78. https://doi.org/10.1016/j.tifs.2003.09.004.
46. Reyher KK, Dufour S, Barkema HW, Des Côteaux L, DeVries TJ, Dohoo IR, Keefe GP, Roy JP, Scholl DT. 2011. The national cohort of dairy farms-a data collection platform for mastitis research in Canada. J Dairy Sci 94:1616-1626. https://doi.org/10.3168/jds.2010-3180.
47. Condas L, De Buck J, Nobrega D, Carson D, Naushad S, Kastelic J, De Vliegher S, Zadoks RN, Middleton J, Dufour S, Barkema HW. 2017. Prevalence of non-aureus staphylococci isolated from milk samples in Canadian dairy herds. J Dairy Sci 100:5592-5612. https://doi.org/10.3168/jds.2016-12478.
48. Schillinger U, Lücke FK. 1989. Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55:1901-1906.
49. Burianek LL, Yousef AE. 2000. Solvent extraction of bacteriocins from liquid cultures. Lett Appl Microbiol 31:193-197. https://doi.org/10.1046/j.1365-2672.2000.00802.x.
50. Köster J, Rahmann S. 2012. Snakemake-a scalable bioinformatics workflow engine. Bioinformatics 28:2520-2522. https://doi.org/10.1093/bioinformatics/bts480.
51. Martin M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet J 17:10-12. https://doi.org/10.14806/ej.17.1.200.
52. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y, Stepanauskas R, Clingenpeel SR, Woyke T, McLean JS, Lasken R, Tesler G, Alekseyev MA, Pevzner PA. 2013. Assembling single-cell genomes and minimetagenomes from chimeric MDA products. J Comput Biol 20:714-737. https://doi.org/10.1089/cmb.2013.0084.
53. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. https://doi.org/10.1093/bioinformatics/btp324.
54. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. https://doi.org/10.1093/bioinformatics/btu153.
55. Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072-1075. https://doi.org/10.1093/bioinformatics/btt086.
56. Priyam A, Woodcroft BJ, Rai V, Munagala A, Moghul I, Ter F, Gibbins MA, Moon H, Leonard G, Rumpf W, Wurm Y. 2015. Sequenceserver: a modern graphical user interface for custom BLAST databases. bioRxiv https://doi.org/10.1101/033142.
57. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W, Breitling R, Takano E, Medema MH. 2015. antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237-W243. https://doi.org/10.1093/nar/gkv437.
58. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH. 2017. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45: D200-D203. https://doi.org/10.1093/nar/gkw1129.
59. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. https://doi.org/10.1093/bioinformatics/bts199.
60. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. https://doi.org/10.1093/bioinformatics/btq461.
61. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772-780. https://doi.org/10.1093/molbev/mst010.
62. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490.
63. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximumlikelihood approach. Mol Biol Evol 18:691-699. https://doi.org/10.1093/oxfordjournals.molbev.a003851.
64. Ozer EA, Allen JP, Hauser AR. 2014. Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt. BMC Genomics 15:737.
65. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. https://doi.org/10.1186/1471-2105-5-113.
66. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. 2009. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191. https://doi.org/10.1093/bioinformatics/btp033.