Proteomes of lactobacillus delbrueckii subsp. bulgaricus LBB.B5 incubated in milk at optimal and low temperatures

mSystems

Volumn 2, Issue 5, 2017, Pages

  Yin, Xiaochen ^a   Salemi, Michelle R ^a   Phinney, Brett S ^a   Gotcheva, Velitchka ^b   Angelov, Angel ^b   Marco, Maria L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF FOOD TECHNOLOGIES   (Bulgaria)

Author keywords

Fermentation; Lactobacillus; Mammalian gut; Proteomics

Indexed keywords

EID: 85041536675     PISSN: None     EISSN: 23795077     Source Type: Journal    
DOI: 10.1128/mSystems.00027-17     Document Type: Article

References (46)

1. Lourens-Hattingh A, Viljoen BC. 2001. Yogurt as probiotic carrier food. Int Dairy J 11:1-17. https://doi.org/10.1016/S0958-6946(01) 00036-X.
2. Driessen FM, Kingma F, Stadhouders J. 1982. Evidence that Lactobacillus bulgaricus in yogurt is stimulated by carbon dioxide produced by Streptococcus thermophilus. Neth Milk Dairy J 36:135-144.
3. Sieuwerts S, de Bok FAM, Hugenholtz J, van Hylckama Vlieg JET. 2008. Unraveling microbial interactions in food fermentations: From classical to genomics approaches. Appl Environ Microbiol 74:4997-5007. https://doi .org/10.1128/AEM.00113-08.
4. Sieuwerts S, Molenaar D, van Hijum SAFT, Beerthuyzen M, Stevens MJA, Janssen PWM, Ingham CJ, de Bok FAM, de Vos WM, van Hylckama Vlieg JET. 2010. Mixed-culture transcriptome analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl Environ Microbiol 76:7775-7784. https://doi .org/10.1128/AEM.01122-10.
5. Astrup A. 2014. Yogurt and dairy product consumption to prevent cardiometabolic diseases: Epidemiologic and experimental studies. Am J Clin Nutr 99:1235S-1242S. https://doi.org/10.3945/ajcn.113.073015.
6. Panahi S, Tremblay A. 2016. The potential role of yogurt in weight management and prevention of type 2 diabetes. J Am Coll Nutr 35: 717-731. https://doi.org/10.1080/07315724.2015.1102103.
7. Pei R, Martin DA, DiMarco DM, Bolling BW. 2017. Evidence for the effects of yogurt on gut health and obesity. Crit Rev Food Sci Nutr 57: 1569-1583. https://doi.org/10.1080/10408398.2014.883356.
8. Shoda T, Futamura M, Yang L, Narita M, Saito H, Ohya Y. 2017. Yogurt consumption in infancy is inversely associated with atopic dermatitis and food sensitization at 5 years of age: A hospital-based birth cohort study. J Dermatol Sci 86:90 -96. https://doi.org/10.1016/j.jdermsci.2017 .01.006.
9. Nestel PJ, Mellett N, Pally S, Wong G, Barlow CK, Croft K, Mori TA, Meikle PJ. 2013. Effects of low-fat or full-fat fermented and non-fermented dairy foods on selected cardiovascular biomarkers in overweight adults. Br J Nutr 110:2242-2249. https://doi.org/10.1017/S0007114513001621.
10. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M, Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health benefits of fermented foods: Microbiota and beyond. Curr Opin Biotechnol 44: 94-102. https://doi.org/10.1016/j.copbio.2016.11.010.
11. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. 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. https://doi.org/10.1038/nrgastro.2014.66.
12. Boudraa G, Benbouabdellah M, Hachelaf W, Boisset M, Desjeux JF, Touhami M. 2001. Effect of feeding yogurt versus milk in children with acute diarrhea and carbohydrate malabsorption. J Pediatr Gastroenterol Nutr 33:307-313. https://doi.org/10.1097/00005176-200109000-00015.
13. Makino S, Ikegami S, Kume A, Horiuchi H, Sasaki H, Orii N. 2010. Reducing the risk of infection in the elderly by dietary intake of yoghurt fermented with Lactobacillus delbrueckii ssp. Bulgaricus OLL1073R-1. Br J Nutr 104:998 -1006. https://doi.org/10.1017/S000711451000173X.
14. Makino S, Sato A, Goto A, Nakamura M, Ogawa M, Chiba Y, Hemmi J, Kano H, Takeda K, Okumura K, Asami Y. 2016. Enhanced natural killer cell activation by exopolysaccharides derived from yogurt fermented with Lactobacillus delbrueckii ssp. Bulgaricus OLL1073R-1. J Dairy Sci 99: 915-923. https://doi.org/10.3168/jds.2015-10376.
15. Moro-García MA, Alonso-Arias R, Baltadjieva M, Fernández Benítez C, Fernández Barrial MA, Díaz Ruisánchez E, Alonso Santos R, Álvarez Sánchez M, Saavedra Miján J, López-Larrea C. 2013. Oral supplementation with Lactobacillus delbrueckii subsp. bulgaricus 8481 enhances systemic immunity in elderly subjects. Age 35:1311-1326. https://doi.org/ 10.1007/s11357-012-9434-6.
16. Hao P, Zheng H, Yu Y, Ding G, Gu W, Chen S, Yu Z, Ren S, Oda M, Konno T, Wang S, Li X, Ji ZS, Zhao G. 2011. Complete sequencing and pangenomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One 6:e15964. https://doi.org/10.1371/journal.pone.0015964.
17. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, Robert C, Oztas S, Mangenot S, Couloux A, Loux V, Dervyn R, Bossy R, Bolotin A, Batto JM, Walunas T, Gibrat JF, Bessières P, Weissenbach J, Ehrlich SD, Maguin E. 2006. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci U S A 103:9274 -9279. https://doi.org/10.1073/pnas .0603024103.
18. Zheng H, Liu E, Shi T, Ye L, Konno T, Oda M, Ji ZS. 2016. Strandspecific RNA-seq analysis of the Lactobacillus delbrueckii subsp. bulgaricus transcriptome. Mol Biosyst 12:508 -519. https://doi.org/10 .1039/c5mb00547g.
19. Rechinger KB, Siegumfeldt H, Svendsen I, Jakobsen M. 2000. 'Early' protein synthesis of Lactobacillus delbrueckii ssp. Bulgaricus in milk revealed by [35S]methionine labeling and two-dimensional gel electrophoresis. Electrophoresis 21:2660 -2669. https://doi.org/10.1002/1522 -2683(20000701)21:13%3C2660::AID-ELPS2660%3E3.0.CO;2-7.
20. Montanari C, Sado Kamdem SL, Serrazanetti DI, Etoa FX, Guerzoni ME. 2010. Synthesis of cyclopropane fatty acids in Lactobacillus helveticus and Lactobacillus sanfranciscensis and their cellular fatty acids changes following short term acid and cold stresses. Food Microbiol 27:493-502. https://doi.org/10.1016/j.fm.2009.12.003.
21. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E. 2002. Stress responses in lactic acid bacteria. Antonie Leeuwenhoek 82:187-216. https://doi.org/10.1023/A:1020631532202.
22. Lee B, Tachon S, Eigenheer RA, Phinney BS, Marco ML. 2015. Lactobacillus casei low-temperature, dairy-associated proteome promotes persistence in the mammalian digestive tract. J Proteome Res 14:3136 -3147. https://doi.org/10.1021/acs.jproteome.5b00387.
23. Marco ML, Tachon S. 2013. Environmental factors influencing the efficacy of probiotic bacteria. Curr Opin Biotechnol 24:207-213. https://doi .org/10.1016/j.copbio.2012.10.002.
24. Sanders ME, Klaenhammer TR, Ouwehand AC, Pot B, Johansen E, Heimbach JT, Marco ML, Tennilä J, Ross RP, Franz C, Pagé N, Pridmore RD, Leyer G, Salminen S, Charbonneau D, Call E, Lenoir-Wijnkoop I. 2014. Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics. Ann N Y Acad Sci 1309:1-18. https://doi .org/10.1111/nyas.12363.
25. Lee B, Yin X, Griffey SM, Marco ML. 2015. Attenuation of colitis by Lactobacillus casei BL23 is dependent on the dairy delivery matrix. Appl Environ Microbiol 81:6425- 6435. https://doi.org/10.1128/AEM.01360-15.
26. Salaün F, Mietton B, Gaucheron F. 2005. Buffering capacity of dairy products. Int Dairy J 15:95-109. https://doi.org/10.1016/j.idairyj.2004.06 .007.
27. Prajapati JB, Nair BM. 2008. The history of fermented foods, p 3-9. In Farnworth ER (ed), Handbook of fermented functional foods, 2nd ed. CRC Press, Boca Raton, FL.
28. Newburg DS, Neubauer S. 1995. Carbohydrates in milks: Analysis, quantities and significance, p 273-249. In Jensen RG (ed), Handbook of milk composition. Academic Press, New York, NY.
29. Wang J, Wu R, Zhang W, Sun Z, Zhao W, Zhang H. 2013. Proteomic comparison of the probiotic bacterium Lactobacillus casei Zhang cultivated in milk and soy milk. J Dairy Sci 96:5603-5624. https://doi.org/10 .3168/jds.2013-6927.
30. Gitton C, Meyrand M, Wang J, Caron C, Trubuil A, Guillot A, Mistou MY. 2005. Proteomic signature of Lactococcus lactis NCDO763 cultivated in milk. Appl Environ Microbiol 71:7152-7163. https://doi.org/10.1128/AEM .71.11.7152-7163.2005.
31. Smeianov VV, Wechter P, Broadbent JR, Hughes JE, Rodríguez BT, Christensen TK, Ardö Y, Steele JL. 2007. Comparative high-density microarray analysis of gene expression during growth of Lactobacillus helveticus in milk versus rich culture medium. Appl Environ Microbiol 73:2661-2672. https://doi.org/10.1128/AEM.00005-07.
32. O'Donovan GA, Neuhard J. 1970. Pyrimidine metabolism in microorganisms. Bacteriol Rev 34:278 -343.
33. Swaisgood HE. 1995. Protein and amino acid composition of bovine milk, p 464-468. In Jensen RG (ed), Handbook of milk composition. Academic Press, New York, NY.
34. Sabahelkheir M, Fat M, Hassan A. 2012. Amino acid composition of human and animal's milk (camel, cow, sheep and goat). ARPN J Sci Technol 2:32-34.
35. Forchhammer K. 2007. Glutamine signalling in bacteria. Front Biosci 12:358 -370. https://doi.org/10.2741/2069.
36. Weissbach H, Etienne F, Hoshi T, Heinemann SH, Lowther WT, Matthews B, St John GS, Nathan C, Brot N. 2002. Peptide methionine sulfoxide reductase: Structure, mechanism of action, and biological function. Arch Biochem Biophys 397:172-178. https://doi.org/10.1006/abbi.2001.2664.
37. Larsen N, Moslehi-Jenabian S, Werner BB, Jensen ML, Garrigues C, Vogensen FK, Jespersen L. 2016. Transcriptome analysis of Lactococcus lactis subsp. lactis during milk acidification as affected by dissolved oxygen and the redox potential. Int J Food Microbiol 226:5-12. https:// doi.org/10.1016/j.ijfoodmicro.2016.03.002.
38. Papadimitriou K, Alegría Á, Bron PA, de Angelis M, Gobbetti M, Kleerebezem M, Lemos JA, Linares DM, Ross P, Stanton C, Turroni F, van Sinderen D, Varmanen P, Ventura M, Zúñiga M, Tsakalidou E, Kok J. 2016. Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80: 837-890. https://doi.org/10.1128/MMBR.00076-15.
39. Jolly L, Stingele F. 2001. Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria. Int Dairy J 11: 733-745. https://doi.org/10.1016/S0958-6946(01)00117-0.
40. Sanders ME, Marco ML. 2010. Food formats for effective delivery of probiotics. Annu Rev Food Sci Technol 1:65- 85. https://doi.org/10.1146/ annurev.food.080708.100743.
41. Marteau P, Minekus M, Havenaar R, Huis In't Veld JHJ. 1997. Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: Validation and the effects of bile. J Dairy Sci 80:1031-1037. https://doi.org/10.3168/jds.S0022-0302(97)76027-2.
42. Tachon S, Lee B, Marco ML. 2014. Diet alters probiotic Lactobacillus persistence and function in the intestine. Environ Microbiol 16: 2915-2926. https://doi.org/10.1111/1462-2920.12297.
43. Yin X, Yan Y, Kim EB, Lee B, Marco ML. 2014. Short communication: Effect of milk and milk containing Lactobacillus casei on the intestinal microbiota of mice. J Dairy Sci 97:2049 -2055. https://doi.org/10.3168/jds.2013 -7477.
44. Käll L, Storey JD, MacCoss MJ, Noble WS. 2008. Assigning significance to peptides identified by tandem mass spectrometry using decoy databases. J Proteome Res 7:29 -34. https://doi.org/10.1021/pr700600n.
45. R Studio. 2012. R Studio: Integrated development environment for R. R Studio, Inc, Boston, MA.
46. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498 -2504. https://doi.org/10.1101/gr.1239303.