A novel lactobacilli-based teat disinfectant for improving bacterial communities in the milks of cow teats with subclinical mastitis

Frontiers in Microbiology

Volumn 8, Issue SEP, 2017, Pages

  Yu, Jie ^a   Ren, Yan ^a   Xi, XiaoXia ^a   Huang, Weiqiang ^a   Zhang, Heping ^a  

^a INNER MONGOLIA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bacterial community; Lactic acid bacteria; SMRT sequencing; Subclinical mastitis; Teat disinfectant

Indexed keywords

DISINFECTANT AGENT; PROBIOTIC AGENT;

ARTICLE; BACTERIAL COUNT; BACTERIUM IDENTIFICATION; CELL COUNTING; CLUSTER ANALYSIS; COMMUNITY STRUCTURE; CONTROLLED STUDY; DNA EXTRACTION; LACTOBACILLUS; LACTOCOCCUS; MASTITIS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MILK; NIPPLE; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SOMATIC CELL;

EID: 85030154416     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01782     Document Type: Article

References (68)

1. Aislabie, J. M., Jordan, S., and Barker, G. M. (2008). Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144, 9-20. doi: 10.1016/j.geoderma.2007.10.006
2. Amir, A., Zeisel, A., Zuk, O., Elgart, M., Stern, S., Shamir, O., et al. (2013). High-resolution microbial community reconstruction by integrating short reads from multiple 16S rRNA regions. Nucleic Acids Res. 41:e205. doi: 10.1093/nar/gkt1070
3. Cao, L. T., Wu, J. Q., Xie, F., Hu, S. H., and Mo, Y. (2007). Efficacy of nisin in treatment of clinical mastitis in lactating dairy cows. J. Dairy Sci. 90, 3980-3985. doi: 10.3168/jds.2007-0153
4. Caporaso, J. G., Bittinger, K., Bushman, F. D., Desantis, T. Z., Andersen, G. L., and Knight, R. (2009). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267. doi: 10.1093/bioinformatics/btp636
5. Cole, J. R., Chai, B., Farris, R. J., Wang, Q., Kulamsyedmohideen, A. S., Mcgarrell, D. M., et al. (2007). The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35(Suppl. 1), 169-172. doi: 10.1093/nar/gkl889
6. Crispie, F., Alonsogómez, M., O'Loughlin, C., Klostermann, K., Flynn, J., Arkins, S., et al. (2008). Intramammary infusion of a live culture for treatment of bovine mastitis: effect of live lactococci on the mammary immune response. J. Dairy Res. 75, 374-384. doi: 10.1017/S0022029908003385
7. Debois, D., Ongena, M., Cawoy, H., and De, P. E. (2013). MALDI-FTICR MS imaging as a powerful tool to identify Paenibacillus antibiotics involved in the inhibition of plant pathogens. J. Am. Soc. Mass Spectrom. 24, 1202-1213. doi: 10.1007/s13361-013-0620-2
8. Dervishi, E., Zhang, G., Dunn, S. M., Mandal, R., Wishart, D. S., and Ametaj, B. N. (2016). GC-MS metabolomics identifies metabolite alterations that precede subclinical mastitis in the blood of transition dairy cows. J. Proteome Res. 16, 433-446. doi: 10.1021/acs.jproteome.6b00538
9. Diepers, A. C., Krömker, V., Zinke, C., Wente, N., Pan, L., Paulsen, K., et al. (2016). In vitro ability of lactic acid bacteria to inhibit mastitis-causing pathogens. Sustain. Chem. Pharm. 5, 84-92. doi: 10.1016/j.scp.2016.06.002
10. Dortet, L., Legrand, P., Soussy, C.-J., and Cattoir, V. (2006). Bacterial identification, clinical significance, and antimicrobial susceptibilities of Acinetobacter ursingii and Acinetobacter schindleri, two frequently misidentified opportunistic pathogens. J. Clin. Microbiol. 44, 4471-4478. doi: 10.1128/JCM.01535-06
11. Doyle, C. J., Gleeson, D., O'Toole, P. W., and Cotter, P. D. (2017). Impacts of seasonal housing and teat preparation on raw milk microbiota: a high-throughput sequencing study. Appl. Environ. Microbiol. 83, e02694-16. doi: 10.1128/AEM.02694-16
12. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
13. Ercolini, D., Russo, F., Ferrocino, I., and Villani, F. (2009). Molecular identification of mesophilic and psychrotrophic bacteria from raw cow's milk. Food Microbiol. 26, 228-231. doi: 10.1016/j.fm.2008.09.005
14. Espeche, M. C., Otero, M. C., Sesma, F., and Nader-Macias, M. E. (2009). Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet. Microbiol. 135, 346-357. doi: 10.1016/j.vetmic.2008.09.078
15. Foret, C. J., Corbellini, C., Young, S., and Janowicz, P. (2005). Efficacy of two iodine teat dips based on reduction of naturally occurring new intramammary infections. J. Dairy Sci. 88, 426-432. doi: 10.3168/jds. S0022-0302(05)72704-1
16. Frola, I. D., Pellegrino, M. S., Espeche, M. C., Giraudo, J. A., Nadermacias, M. E., and Bogni, C. I. (2011). Effects of intramammary inoculation of Lactobacillus perolens CRL1724 in lactating cows' udders. J. Dairy Res. 79, 84-92. doi: 10.1017/S0022029911000835
17. Galton, D. M., Petersson, L. G., and Erb, H. N. (1986). Milk iodine residues in herds practicing iodophor premilking teat disinfection. J. Dairy Sci. 69, 267-271. doi: 10.3168/jds. S0022-0302(86)80397-6
18. Gibson, H., Sinclair, L. A., Brizuela, C. M., Worton, H. L., and Protheroe, R. G. (2008). Effectiveness of selected premilking teat-cleaning regimes in reducing teat microbial load on commercial dairy farms. Lett. Appl. Microbiol. 46, 295-300. doi: 10.1111/j.1472-765X.2007.02308.x
19. Griffiths, M. W., and Phillips, J. D. (1990). Incidence, source and some properties of psychrotrophic Bacillus spp found in raw and pasteurized milk. Int. J. Dairy Technol. 43, 62-66. doi: 10.1111/j.1471-0307.1990.tb02446.x
20. Hammer,Ø, and Harper, D. A. T. (2009). Past: paleontological statistics software package for educaton and data anlysis. Palaeontol. Electron 4, 1-9.
21. Hildebrandt, U., Ouziad, F., Marner, F. J., and Bothe, H. (2006). The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol. Lett. 254, 258-267. doi: 10.1111/j.1574-6968.2005.00027.x
22. Hillerton, J. E. (1999). Redefining Mastitis Based on Somatic Cell Count. Brussels: International Dairy Federation, 4-6.
23. Hou, Q., Xu, H., Zheng, Y., Xi, X., Kwok, L. Y., Sun, Z., et al. (2015). Evaluation of bacterial contamination in raw milk, ultra-high temperature milk and infant formula using single molecule, real-time sequencing technology. J. Dairy Sci. 98, 8464-8472. doi: 10.3168/jds.2015-9886
24. Ingawa, K. H., Adkinson, R. W., and Gough, R. H. (1992). Evaluation of a gel teat cleaning and sanitizing compound for premilking hygiene. J. Dairy Sci. 75, 1224-1232. doi: 10.3168/jds. S0022-0302(92)77871-0
25. Kämpfer, P., Falsen, E., and Busse, H. J. (2008). Naxibacter varians sp. nov. and Naxibacter haematophilus sp. nov., and emended description of the genus Naxibacter. Int. J. Syst. Evol. Microbiol. 58, 1680-1684. doi: 10.1099/ijs.0.65516-0
26. Kim, Y. G., Choi, D. H., Hyun, S., and Cho, B. C. (2007). Oceanobacillus profundus sp. nov., isolated from a deep-sea sediment core. Int. J. Syst. Evol. Microbiol. 57, 409-413. doi: 10.1099/ijs.0.64375-0
27. Klostermann, K., Crispie, F., Flynn, J., Meaney, W. J., Paul, R. R., and Hill, C. (2010). Efficacy of a teat dip containing the bacteriocin lacticin 3147 to eliminate Gram-positive pathogens associated with bovine mastitis. J. Dairy Res. 77, 231-238. doi: 10.1017/S0022029909990239
28. Kuehn, J. S., Gorden, P. J., Munro, D., Rong, R., Dong, Q., Plummer, P. J., et al. (2013). Bacterial community profiling of milk samples as a means to understand culture-negative bovine clinical mastitis. PLOS ONE 8:e61959. doi: 10.1371/journal.pone.0061959
29. Kummee, P., Borisutpeth, M., Chanlun, S., Kanbutra, P., and Chanlun, A. (2015). Efficacy of guava leaf extract as alternative pre-milking teat dipping in reducing teat-end bacterial load of milking dairy cows. Int. J. Pharm. Pharm. Sci. 7, 434-438.
30. Lafarge, V., Ogier, J. C., Girard, V., Maladen, V., Leveau, J. Y., Gruss, A., et al. (2004). Raw cow milk bacterial population shifts attributable to refrigeration. Appl. Environ. Microbiol. 70, 5644-5650. doi: 10.1128/AEM.70.9.5644-5650.2004
31. Li, D., Rothballer, M., Schmid, M., Esperschütz, J., and Hartmann, A. (2011). Acidovorax radicis sp. nov., a wheat-root-colonizing bacterium. Int. J. Syst. Evol. Microbiol. 61, 2589-2594. doi: 10.1099/ijs.0.025296-0
32. Li, L., Renye, J. A. Jr., Feng, L., Zeng, Q., Tang, Y., Huang, L., et al. (2016). Characterization of the indigenous microflora in raw and pasteurized buffalo milk during storage at refrigeration temperature by high-throughput sequencing. J. Dairy Sci. 99, 7016-7024. doi: 10.3168/jds.2016-11041
33. Lindquist, D., Murrill, D., Burran, W. P., Winans, G., Janda, J. M., and Probert, W. (2003). Characteristics of Massilia timonae and Massilia timonae-like isolates from human patients, with an emended description of the species. J. Clin. Microbiol. 41, 192-196. doi: 10.1128/JCM.41.1.192-196.2003
34. Liu, W., Zheng, Y., Kwok, L. Y., Sun, Z., Zhang, J., Guo, Z., et al. (2015). High-throughput sequencing for the detection of the bacterial and fungal diversity in Mongolian naturally fermented cow's milk in Russia. BMC Microbiol. 15:45. doi: 10.1186/s12866-015-0385-9
35. Lozupone, C., Hamady, M., and Knight, R. (2006). UniFrac-An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371. doi: 10.1186/1471-2105-7-371
36. Lozupone, C., and Knight, R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235. doi: 10.1128/AEM.71.12.8228-8235.2005
37. Ma, C., Zhao, J., Xi, X., Ding, J., Wang, H., Zhang, H., et al. (2015). Bovine mastitis may be associated with the deprivation of gut Lactobacillus. Benef. Microbes 7, 95-102. doi: 10.3920/BM2015.0048
38. Mojgani, N., and Ashtiani, M. P. (2006). In vitro inhibition of mastitis pathogens by bacteriocin RN 86 produced by an indigenous Lactobacillus casei isolate. J. Appl. Sci. 6, 2629-2634. doi: 10.3923/jas.2006.2629.2634
39. Monsallier, F., Verdier-Metz, I., Agabriel, C., Martin, B., and Montel, M. C. (2012). Variability of microbial teat skin flora in relation to farming practices and individual dairy cow characteristics. Dairy Sci. Technol. 92, 265-278. doi: 10.1007/s13594-012-0064-7
40. Mosher, J. J., Bernberg, E. L., Shevchenko, O., Kan, J., and Kaplan, L. A. (2013). Efficacy of a 3rd generation high-throughput sequencing platform for analyses of 16S rRNA genes from environmental samples. J. Mirobiol. Methods 95, 175-181. doi: 10.1016/j.mimet.2013.08.009
41. Nemec, A., De Baere, T., Tjernberg, I., Vaneechoutte, M., van der Reijden, T. J., and Dijkshoorn, L. (2001). Acinetobacter ursingii sp. nov. and Acinetobacter schindleri sp. nov., isolated from human clinical specimens. Int. J. Syst. Evol. Microbiol. 51, 1891-1899. doi: 10.1099/00207713-51-5-1891
42. Oikonomou, G., Bicalho, M. L., Meira, E., Rossi, R. E., Foditsch, C., Machado, V. S., et al. (2014). Microbiota of cow's milk; distinguishing healthy, sub-clinically and clinically diseased quarters. PLOS ONE 9:e85904. doi: 10.1371/journal.pone.0085904
43. Oliver, S. P., Boor, K. J., Murphy, S. C., Murinda, S. E., and Callaway, T. R. (2009). Food safety hazards associated with consumption of raw milk. Foodborne Pathog. Dis. 6, 793-806. doi: 10.1089/fpd.2009.0302
44. Oliver, S. P., Lewis, M. J., Ingle, T. L., Gillespie, B. E., Matthews, K. R., and Dowlen, H. H. (1993). Premilking teat disinfection for the prevention of environmental pathogen intramammary infections. J. Food Protect. 56, 852-855. doi: 10.4315/0362-028X-56.10.852
45. Oyaizu, H., Stackebrandt, E., Schleifer, K. H., Ludwig, W., Pohla, H., Hirata, A., et al. (1987). A radiation-resistant rod-shaped bacterium, Deinobacter grandis gen. nov., sp. nov., with peptidoglycan containing ornithine. Int. J. Syst. Bacteriol. 37, 62-67. doi: 10.1099/00207713-37-1-62
46. Price, M. N., Dehal, P. S., and Arkin, A. P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650. doi: 10.1093/molbev/msp077
47. Quigley, L., O'Sullivan, O., Stanton, C., Beresford, T. P., Ross, R. P., Fitzgerald, G. F., et al. (2013). The complex microbiota of raw milk. FEMS Microbiol. Rev. 37, 664-698. doi: 10.1111/1574-6976.12030
48. Rainard, P. (2017). Mammary microbiota of dairy ruminants: fact or fiction? Vet. Res. 48, 25. doi: 10.1186/s13567-017-0429-2
49. Ranieri, M. L., Ivy, R. A., Mitchell, W. R., Call, E., Masiello, S. N., Wiedmann, M., et al. (2012). Real-Time PCR detection of Paenibacillus spp. in raw milk to predict shelf life performance of pasteurized fluid milk products. Appl. Environ. Microbiol. 78, 5855-5863. doi: 10.1128/AEM.01361-12
50. Rodrigues, M. X., Lima, S. F., Canniatti-Brazaca, S. G., and Bicalho, R. C. (2017). The microbiome of bulk tank milk: characterization and associations with somatic cell count and bacterial count. J. Dairy Sci. 100, 2536-2552. doi: 10.3168/jds.2016-11540
51. Schukken, Y. H., Wilson, D. J., Welcome, F., Garrison-Tikofsky, L., and Gonzalez, R. N. (2003). Monitoring udder health and milk quality using somatic cell counts. Vet. Res. 34, 579-596. doi: 10.1051/vetres:2003028
52. Sharma, N., Gupta, S. K., Sharma, U., and Hussain, K. (2007). Treatment of clinical mastitis in buffalo-A case report. Buffalo Bull. 26, 56-58.
53. Sharma, N., and Jeong, D. K. (2013). Stem cell research: a novel boulevard towards improved bovine mastitis management. Int. J. Biol. Sci. 9, 819-829. doi: 10.7150/ijbs.6901
54. Soleimani, N. A., Kermanshahi, R. K., Yakhchali, B., and Sattari, T. N. (2010). Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afr. J. Microbiol. Res. 420, 2169-2173.
55. Spring, S., Kämpfer, P., and Schleifer, K. H. (2001). Limnobacter thiooxidans gen. nov., sp. nov., a novel thiosulfate-oxidizing bacterium isolated from freshwater lake sediment. Int. J. Syst. Evol. Microbiol. 51, 1463-1470. doi: 10.1099/00207713-51-4-1463
56. Suriyasathaporn, W., and Chupia, V. (2011). Reduction in numbers of bacteria after pre-milking teat dipping in milking dairy cows. CMU. J. Nat. Sci. 10, 301-306.
57. Tagg, J. R., and Dierksen, K. P. (2003). Bacterial replacement therapy: adapting 'germ warfare' to infection prevention. Trends Biotechnol. 21, 217-223. doi: 10.1016/S0167-7799(03)00085-4
58. Vacheyrou, M., Normand, A. C., Guyot, P., Cassagne, C., Piarroux, R., and Bouton, Y. (2011). Cultivable microbial communities in raw cow milk and potential transfers from stables of sixteen French farms. Int. J. Food Microbiol. 146, 253-262. doi: 10.1016/j.ijfoodmicro.2011.02.033
59. Verdiermetz, I., Gagne, G., Bornes, S., Monsallier, F., Veisseire, P., Delbèspaus, C., et al. (2012). Cow teat skin, a potential source of diverse microbial populations for cheese production. Appl. Environ. Microbiol. 78, 326-333. doi: 10.1128/AEM.06229-11
60. Wu, S. Y., Li, I. C., Lin, Y. C., and Chen, C. C. (2016). Characterization and safety evaluation of Deinococcus grandis as feed additive for hens. Regul. Toxicol. Pharm. 76, 121-127. doi: 10.1016/j.yrtph.2016.01.019
61. Yezli, W., Zebboudj-Yezli, N., Hamini-Kadar, N., Kihal, M., and Henni, J. E. (2015). An in vitro antagonistic activity evaluation of rhizobacteria against Fusarium oxysporum f. sp. radicis-lycopersici (Forl) isolated from the Algerian west. Int. J. Biosci. 7, 95-103. doi: 10.12692/ijb/7.1.95-103
62. Yu, H. J., Chen, Y. F., Yang, H. J., Yang, J., Xue, J. G., Li, C. K., et al. (2015). Screening for Lactobacillus plantarum with potential inhibitory activity against enteric pathogens. Ann. Microbiol. 65, 1-9. doi: 10.1007/s13213-014-0963-3
63. Yu, J., Gao, W., Qing, M., Sun, Z., Wang, W., Liu, W., et al. (2012). Identification and characterization of lactic acid bacteria isolated from traditional pickles in Sichuan, China. J. Gen. Appl. Microbiol. 58, 163-172. doi: 10.2323/jgam.58.163
64. Zeedan, G. S. G., Abdalhamed, A. M., Abdeen, E., Ottai, M. E., and Abdelshafy, S. (2014). Evaluation of antibacterial effect of some Sinai medicinal plant extracts on bacteria isolated from bovine mastitis. Vet. World 7, 991-998. doi: 10.14202/vetworld.2014.991-998
65. Zhang, R., Huo, W., Zhu, W., and Mao, S. (2015). Characterization of bacterial community of raw milk from dairy cows during subacute ruminal acidosis challenge by high-throughput sequencing. J. Sci. Food Agric. 95, 1072-1079. doi: 10.1002/jsfa.6800
66. Zheng, Y., Xi, X., Xu, H., Hou, Q., Bian, Y., Yu, Z., et al. (2016). Using PacBio long-read high-throughput microbial gene amplicon sequencing to evaluate infant formula safety. J. Agric. Food Chem. 64, 6993-7001. doi: 10.1021/acs.jafc.6b01817
67. Ziarno, M., and Zareba, D. (2010). Characteristics and occurrence of Paenibacillus bacteria in milk and milk products. Med. Weter 66, 600-603.
68. Zucali, M., Bava, L., Tamburini, A., Brasca, M., Vanoni, L., and Sandrucci, A. (2011). Effects of season, milking routine and cow cleanliness on bacterial and somatic cell counts of bulk tank milk. J. Dairy Res. 78, 436-441. doi: 10.1017/S0022029911000598