Absolute enumeration of probiotic strains lactobacillus acidophilus NCFM® and Bifidobacterium animalis subsp. lactis Bl-04® via chip-based digital PCR

Frontiers in Microbiology

Volumn 9, Issue APR, 2018, Pages

  Hansen, Sarah J Z ^a   Morovic, Wesley ^a   DeMeules, Martha ^a   Stahl, Buffy ^a   Sindelar, Connie W ^a  

^a DUPONT COMPANY   (United States)

Author keywords

Bifidobacterium animalis subsp. lactis Bl 04; Chip based digital PCR; Enumeration; Lactobacillus acidophilus NCFM; Plate count; Probiotic; Propidium monoazide

Indexed keywords

PROBIOTIC AGENT; VERY LONG CHAIN FATTY ACID;

ANALYSIS OF VARIANCE; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM ANIMALIS; BIOINFORMATICS; CELL COUNTING; CELL VIABILITY ASSAY; COLONY FORMING UNIT; CONTROLLED STUDY; CORRELATION COEFFICIENT; DNA ISOLATION; DNA SEQUENCE; DRUG RELEASE; FLOW CYTOMETRY; FREEZE DRYING; GENE AMPLIFICATION; INCUBATION TEMPERATURE; LABORATORY; LACTOBACILLUS ACIDOPHILUS; LIMIT OF QUANTITATION; LITERATURE; MICROSCOPY; NONHUMAN; POLYMERASE CHAIN REACTION; TECHNOLOGY; TEMPERATURE; VALIDATION PROCESS;

EID: 85045266792     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.00704     Document Type: Article

References (72)

1. Achtman, M. (2008). Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu. Rev. Microbiol. 62, 53-70. doi: 10.1146/annurev.micro.62.081307.162832
2. Altermann, E., Russell, W. M., Azcarate-Peril, M. A., Barrangou, R., Buck, B. L., McAuliffe, O., et al. (2005). Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. U.S.A. 102, 3906-3912. doi: 10.1073/pnas.0409188102
3. Amor, K. B., Vaughan, E. E., and de Vos, W. M. (2007). Advanced molecular tools for the identification of lactic acid bacteria. J. Nutr. 137, 741S-747S
4. Barbau-Piednoir, E., Mahillon, J., Pillyser, J., Coucke, W., Roosens, N. H., and Botteldoorn, N. (2014). Evaluation of viability-qPCR detection system on viable and dead Salmonella serovar Enteritidis. J. Microbiol. Methods 103, 131-137. doi: 10.1016/j.mimet.2014.06.003
5. Barrangou, R., Briczinski, E. P., Traeger, L. L., Loquasto, J. R., Richards, M., Horvath, P., et al. (2009). Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J. Bacteriol. 191, 4144-4151. doi: 10.1128/JB.00155-09
6. Best Practices Guidelines for Probiotics | Council for Responsible Nutrition (2017). Available at: https://www.crnusa.org/self-regulation/voluntary-guidelines-best-practices/best-practices-guidelines-probiotics [Accessed July 26, 2017]
7. Blaya, J., Lloret, E., Santísima-Trinidad, A. B., Ros, M., and Pascual, J. A. (2016). Molecular methods (digital PCR and real-time PCR) for the quantification of low copy DNA of Phytophthora nicotianae in environmental samples: digital PCR: a new method to quantify P. nicotianae. Pest Manag. Sci. 72, 747-753. doi: 10.1002/ps.4048
8. Briczinski, E. P., Loquasto, J. R., Barrangou, R., Dudley, E. G., Roberts, A. M., and Roberts, R. F. (2009). Strain-specific genotyping of Bifidobacterium animalis subsp. lactis by using single-nucleotide polymorphisms, insertions, and deletions. Appl. Environ. Microbiol. 75, 7501-7508. doi: 10.1128/AEM.01430-09
9. Bunthof, C. J., Bloemen, K., Breeuwer, P., Rombouts, F. M., and Abee, T. (2001). Flow cytometric assessment of viability of lactic acid bacteria. Appl. Environ. Microbiol. 67, 2326-2335. doi: 10.1128/AEM.67.5.2326-2335.2001
10. Bustin, S. A. (2004). A-Z of Quantitative PCR. La Jolla, CA: International University Line
11. Champagne, C. P., Ross, R. P., Saarela, M., Hansen, K. F., and Charalampopoulos, D. (2011). Recommendations for the viability assessment of probiotics as concentrated cultures and in food matrices. Int. J. Food Microbiol. 149, 185-193. doi: 10.1016/j.ijfoodmicro.2011.07.005
12. Codony, F., Agustí, G., and Allué-Guardia, A. (2015). Cell membrane integrity and distinguishing between metabolically active and inactive cells as a means of improving viability PCR. Mol. Cell. Probes 29, 190-192. doi: 10.1016/j.mcp.2015.03.003
13. Corry, J. E. L., Jarvis, B., Passmore, S., and Hedges, A. (2007). A critical review of measurement uncertainty in the enumeration of food micro-organisms. Food Microbiol. 24, 230-253. doi: 10.1016/j.fm.2006.05.003
14. Dave, R. I., and Shah, N. P. (1996). Evaluation of media for selective enumeration of Streptococcus thermophilus, Lactobacillus delbrueckii ssp. bulgaricus, Lactobacillus acidophilus, and Bifidobacteria. J. Dairy Sci. 79, 1529-1536. doi: 10.3168/jds. S0022-0302(96)76513-X
15. Davis, C. (2014). Enumeration of probiotic strains: review of culture-dependent and alternative techniques to quantify viable bacteria. J. Microbiol. Methods 103, 9-17. doi: 10.1016/j.mimet.2014.04.012
16. de Ruig, W. G. (1996). Characterizing and optimizing analytical method quality. Trends Food Sci. Technol. 7, 234-240. doi: 10.1016/0924-2244(96)20004-4
17. Desfossés-Foucault, é., Dussault-Lepage, V., Le Boucher, C., Savard, P., LaPointe, G., and Roy, D. (2012). Assessment of probiotic viability during Cheddar cheese manufacture and ripening using propidium monoazide-PCR quantification. Front. Microbiol. 3:350. doi: 10.3389/fmicb.2012.00350
18. Dinu, L.-D., and Bach, S. (2013). Detection of viable but non-culturable Escherichia coli O157:H7 from vegetable samples using quantitative PCR with propidium monoazide and immunological assays. Food Control 31, 268-273. doi: 10.1016/j.foodcont.2012.10.020
19. Erkus, O., de Jager, V. C. L., Geene, R. T. C. M., van Alen-Boerrigter, I., Hazelwood, L., van Hijum, S. A. F. T., et al. (2016). Use of propidium monoazide for selective profiling of viable microbial cells during Gouda cheese ripening. Int. J. Food Microbiol. 228, 1-9. doi: 10.1016/j.ijfoodmicro.2016.03.027
20. Fittipaldi, M., Nocker, A., and Codony, F. (2012). Progress in understanding preferential detection of live cells using viability dyes in combination with DNA amplification. J. Microbiol. Methods 91, 276-289. doi: 10.1016/j.mimet.2012.08.007
21. Foerst, P., and Santivarangkna, C. (2015). Advances in Probiotic Technology. Boca Raton, FL: CRC Press. doi: 10.1201/b18807
22. Galat, A., Dufresne, J., Combrisson, J., Thépaut, J., Boumghar-Bourtchai, L., Boyer, M., et al. (2016). Novel method based on chromogenic media for discrimination and selective enumeration of lactic acid bacteria in fermented milk products. Food Microbiol. 55, 86-94. doi: 10.1016/j.fm.2015.11.005
23. García-Cayuela, T., Tabasco, R., Peláez, C., and Requena, T. (2009). Simultaneous detection and enumeration of viable lactic acid bacteria and bifidobacteria in fermented milk by using propidium monoazide and real-time PCR. Int. Dairy J. 19, 405-409. doi: 10.1016/j.idairyj.2009.02.001
24. Hayden, R. T., Gu, Z., Sam, S. S., Sun, Y., Tang, L., Pounds, S., et al. (2016). Comparative performance of reagents and platforms for quantitation of cytomegalovirus DNA by digital PCR. J. Clin. Microbiol. 54, 2602-2608. doi: 10.1128/JCM.01474-16
25. Heid, C. A., Stevens, J., Livak, K. J., and Williams, P. M. (1996). Real time quantitative PCR. Genome Res. 6, 986-994. doi: 10.1101/gr.6.10.986
26. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., et al. (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506-514. doi: 10.1038/nrgastro.2014.66
27. ISO 19344| IDF 232 (2015). Milk and Milk Products-Starter Cultures, Probiotics and Fermented Products-Quantification of Lactic Acid Bacteria by Flow Cytometry. Geneva: ISO
28. Jacobs, B. K. M., Goetghebeur, E., Vandesompele, J., De Ganck, A., Nijs, N., Beckers, A., et al. (2017). Model-based classification for digital PCR: your umbrella for rain. Anal. Chem. 89, 4461-4467. doi: 10.1021/acs.analchem.6b04208
29. Jongenburger, I., Reij, M. W., Boer, E. P. J., Gorris, L. G. M., and Zwietering, M. H. (2010). Factors influencing the accuracy of the plating method used to enumerate low numbers of viable micro-organisms in food. Int. J. Food Microbiol. 143, 32-40. doi: 10.1016/j.ijfoodmicro.2010.07.025
30. Kharchenko, N. V., Cherdynceva, T. A., and Netrusov, A. I. (2017). Development of lyophilization procedure ensuring survival of bifidobacteria and preservation of their probiotic potential upon long-term storage. Microbiology 86, 225-230. doi: 10.1134/S0026261717020102
31. Kinz, E., Leiherer, A., Lang, A. H., Drexel, H., and Muendlein, A. (2015). Accurate quantitation of JAK2 V617F allele burden by array-based digital PCR. Int. J. Lab. Hematol. 37, 217-224. doi: 10.1111/ijlh.12269
32. Kolacek, S., Hojsak, I., Berni Canani, R., Guarino, A., Indrio, F., Orel, R., et al. (2017). Commercial probiotic products: a call for improved quality control. A Position Paper by the ESPGHAN Working Group for Probiotics and Prebiotics. J. Pediatr. Gastroenterol. Nutr. 65, 117-124. doi: 10.1097/MPG.0000000000001603
33. Koressaar, T., and Remm, M. (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289-1291. doi: 10.1093/bioinformatics/btm091
34. Kramer, M., Obermajer, N., Bogovic Matijašic, B., Rogelj, I., and Kmetec, V. (2009). Quantification of live and dead probiotic bacteria in lyophilised product by real-time PCR and by flow cytometry. Appl. Microbiol. Biotechnol. 84, 1137-1147. doi: 10.1007/s00253-009-2068-7
35. Lahtinen, S. J. (2012). Probiotic viability-does it matter? Microb. Ecol. Health Dis. 2012:23. doi: 10.3402/mehd.v23i0.18567
36. Lahtinen, S. J., Ahokoski, H., Reinikainen, J. P., Gueimonde, M., Nurmi, J., Ouwehand, A. C., et al. (2008). Degradation of 16S rRNA and attributes of viability of viable but nonculturable probiotic bacteria. Lett. Appl. Microbiol. 46, 693-698. doi: 10.1111/j.1472-765X.2008.02374.x
37. Leifels, M., Jurzik, L., Wilhelm, M., and Hamza, I. A. (2015). Use of ethidium monoazide and propidium monoazide to determine viral infectivity upon inactivation by heat, UV-exposure and chlorine. Int. J. Hyg. Environ. Health 218, 686-693. doi: 10.1016/j.ijheh.2015.02.003
38. Li, Z., Liu, Y., Wei, Q., Liu, Y., Liu, W., Zhang, X., et al. (2016). Picoliter well array chip-based digital recombinase polymerase amplification for absolute quantification of nucleic acids. PLoS One 11:e0153359. doi: 10.1371/journal.pone.0153359
39. Lomonaco, S., Furumoto, E. J., Loquasto, J. R., Morra, P., Grassi, A., and Roberts, R. F. (2015). Development of a rapid SNP-typing assay to differentiate Bifidobacterium animalis ssp. lactis strains used in probiotic-supplemented dairy products. J. Dairy Sci. 98, 804-812. doi: 10.3168/jds.2014-8509
40. MacCannell, D. (2013). Bacterial strain typing. Clin. Lab. Med. 33, 629-650. doi: 10.1016/j.cll.2013.03.005
41. Malinen, E., Kassinen, A., Rinttilä, T., and Palva, A. (2003). Comparison of real-time PCR with SYBR Green I or 5'-nuclease assays and dot-blot hybridization with rDNA-targeted oligonucleotide probes in quantification of selected faecal bacteria. Microbiology 149, 269-277. doi: 10.1099/mic.0.25975-0
42. Masco, L., Vanhoutte, T., Temmerman, R., Swings, J., and Huys, G. (2007). Evaluation of real-time PCR targeting the 16S rRNA and recA genes for the enumeration of bifidobacteria in probiotic products. Int. J. Food Microbiol. 113, 351-357. doi: 10.1016/j.ijfoodmicro.2006.07.021
43. Matulka, R. (2016). Probiotics: The Claimed Effect Decides the Regulatory Path. Available at: https://www.naturalproductsinsider.com/articles/2016/01/probiotics-the-claimed-effect-decides-the-regulat.aspx
44. McOrist, A. L., Jackson, M., and Bird, A. R. (2002). A comparison of five methods for extraction of bacterial DNA from human faecal samples. J. Microbiol. Methods 50, 131-139. doi: 10.1016/S0167-7012(02)00018-0
45. Mills, S., Stanton, C., Fitzgerald, G. F., and Ross, R. P. (2011). Enhancing the stress responses of probiotics for a lifestyle from gut to product and back again. Microb. Cell Fact. 10:S19. doi: 10.1186/1475-2859-10-S1-S19
46. Morovic, W., Hibberd, A. A., Zabel, B., Barrangou, R., and Stahl, B. (2016). Genotyping by PCR and high-throughput sequencing of commercial probiotic products reveals composition biases. Front. Microbiol. 7:1747. doi: 10.3389/fmicb.2016.01747
47. Mullis, K. B., and Faloona, F. A. (1987). [21] Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155, 335-350. doi: 10.1016/0076-6879(87)55023-6
48. Mumy, K. L., and Findlay, R. H. (2004). Convenient determination of DNA extraction efficiency using an external DNA recovery standard and quantitative-competitive PCR. J. Microbiol. Methods 57, 259-268. doi: 10.1016/j.mimet.2004.01.013
49. Nkuipou-Kenfack, E., Engel, H., Fakih, S., and Nocker, A. (2013). Improving efficiency of viability-PCR for selective detection of live cells. J. Microbiol. Methods 93, 20-24. doi: 10.1016/j.mimet.2013.01.018
50. Nocker, A., Sossa, K. E., and Camper, A. K. (2007a). Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 70, 252-260. doi: 10.1016/j.mimet.2007.04.014
51. Nocker, A., Sossa-Fernandez, P., Burr, M. D., and Camper, A. K. (2007b). Use of propidium monoazide for live/dead distinction in microbial ecology. Appl. Environ. Microbiol. 73, 5111-5117. doi: 10.1128/AEM.02987-06
52. Oberg, C. J., Moyes, L. V., Domek, M. J., Brothersen, C., and McMahon, D. J. (2011). Survival of probiotic adjunct cultures in cheese and challenges in their enumeration using selective media. J. Dairy Sci. 94, 2220-2230. doi: 10.3168/jds.2010-3934
53. Ottesen, E. A., Hong, J. W., Quake, S. R., and Leadbetter, J. R. (2006). Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314, 1464-1467. doi: 10.1126/science.1131370
54. Ouwehand, A. C., and Salminen, S. J. (1998). The health effects of cultured milk products with viable and non-viable bacteria. Int. Dairy J. 8, 749-758. doi: 10.1016/S0958-6946(98)00114-9
55. Patro, J. N., Ramachandran, P., Barnaba, T., Mammel, M. K., Lewis, J. L., and Elkins, C. A. (2016). Culture-independent metagenomic surveillance of commercially available probiotics with high-throughput next-generation sequencing. mSphere 1, e00057-16. doi: 10.1128/mSphere.00057-16
56. Poddar, D., Das, S., Jones, G., Palmer, J., Jameson, G. B., Haverkamp, R. G., et al. (2014). Stability of probiotic Lactobacillus paracasei during storage as affected by the drying method. Int. Dairy J. 39, 1-7. doi: 10.1016/j.idairyj.2014.04.007
57. Probiotic Ingredients Market worth 46.55 Billion Usd by 2020 (2017). Available at http://www.marketsandmarkets.com/PressReleases/probiotics.asp [Accessed July 24, 2017]
58. Ricchi, M., Bertasio, C., Boniotti, M. B., Vicari, N., Russo, S., Tilola, M., et al. (2017). Comparison among the quantification of bacterial pathogens by qPCR, dPCR, and cultural methods. Front. Microbiol. 8:1174. doi: 10.3389/fmicb.2017.01174
59. Sanders, R., Huggett, J. F., Bushell, C. A., Cowen, S., Scott, D. J., and Foy, C. A. (2011). Evaluation of digital PCR for absolute DNA quantification. Anal. Chem. 83, 6474-6484. doi: 10.1021/ac103230c
60. Sefrioui, D., Sarafan-Vasseur, N., Beaussire, L., Baretti, M., Gangloff, A., Blanchard, F., et al. (2015). Clinical value of chip-based digital-PCR platform for the detection of circulating DNA in metastatic colorectal cancer. Dig. Liver Dis. 47, 884-890. doi: 10.1016/j.dld.2015.05.023
61. Shah, N. P. (2000). Probiotic bacteria: selective enumeration and survival in dairy foods. J. Dairy Sci. 83, 894-907. doi: 10.3168/jds. S0022-0302(00)74953-8
62. Stahl, B., and Barrangou, R. (2013). Complete genome sequence of Probiotic strain Lactobacillus acidophilus La-14. Genome Announc. 1:e00376-13. doi: 10.1128/genomeA.00376-13
63. Staley, J. T. (2006). The bacterial species dilemma and the genomic-phylogenetic species concept. Philos. Trans. R. Soc. B Biol. Sci. 361, 1899-1909. doi: 10.1098/rstb.2006.1914
64. Temmerman, R., Pot, B., Huys, G., and Swings, J. (2003). Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int. J. Food Microbiol. 81, 1-10. doi: 10.1016/S0168-1605(02)00162-9
65. Tripathi, M. K., and Giri, S. K. (2014). Probiotic functional foods: survival of probiotics during processing and storage. J. Funct. Foods 9, 225-241. doi: 10.1016/j.jff.2014.04.030
66. U.S. Food & Drug Administration. (2008). Dietary Supplements-Guidance for Industry: Substantiation for Dietary Supplement Claims Made Under Section 403(r) (6) of the Federal Food, Drug, and Cosmetic Act. Available at: https://www.fda.gov/food/guidanceregulation/guidancedocumentsregulatoryinformation/dietarysupplements/ucm073200.htm
67. United States Pharmacopeial Convention. (2015). Food Chemicals Codex, 9th Edn, Suppl. 3. Rockville, MD: United States Pharmacopeial Convention
68. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., et al. (2012). Primer3-new capabilities and interfaces. Nucleic Acids Res. 40:e115. doi: 10.1093/nar/gks596
69. Volkert, M., Ananta, E., Luscher, C., and Knorr, D. (2008). Effect of air freezing, spray freezing, and pressure shift freezing on membrane integrity and viability of Lactobacillus rhamnosus GG. J. Food Eng. 87, 532-540. doi: 10.1016/j.jfoodeng.2008.01.008
70. Wang, D., Yamahara, K. M., Cao, Y., and Boehm, A. B. (2016). Absolute quantification of enterococcal 23S rRNA gene using digital PCR. Environ. Sci. Technol. 50, 3399-3408. doi: 10.1021/acs.est.5b05747
71. Zárate, G., and Nader-Macias, M. E. (2006). Viability and biological properties of probiotic vaginal lactobacilli after lyophilization and refrigerated storage into gelatin capsules. Process Biochem. 41, 1779-1785. doi: 10.1016/j.procbio.2006.03.024
72. Zhang, C., and Xing, D. (2007). Miniaturized PCR chips for nucleic acid amplification and analysis: latest advances and future trends. Nucleic Acids Res. 35, 4223-4237. doi: 10.1093/nar/gkm389