New genes involved in mild stress response identified by transposon mutagenesis in Lactobacillus paracasei

Frontiers in Microbiology

Volumn 9, Issue MAR, 2018, Pages

  Palud, Aurore ^a   Scornec, Hélène ^a   Cavin, Jean François ^a   Licandro, Hélène ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Bacterial adaptation; Lactic acid bacteria; Mild stresses; Stress response genes; Transposon mutants

Indexed keywords

BIOLOGICAL MARKER;

ARTICLE; BACTERIAL GENETICS; BACTERIAL VIABILITY; CARBOHYDRATE METABOLISM; CELLULAR STRESS RESPONSE; DISK DIFFUSION; GROWTH INHIBITION; HEAT STRESS; LACTOBACILLUS PARACASEI; MUTAGENESIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS; TRANSPOSON; TURBIDIMETRY; UPREGULATION; WILD TYPE;

EID: 85044343072     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.00535     Document Type: Article

References (50)

1. Alcántara, C., Zúñiga, M. (2012). Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23. Microbiology 158, 1206-1218. doi: 10.1099/mic.0.055657-0.
2. Andrade-Linares, D. R., Lehmann, A., Rillig, M. C. (2016). Microbial stress priming: a meta-analysis: microbial priming to stress. Environ. Microbiol. 18, 1277-1288. doi: 10.1111/1462-2920.13223.
3. Beaufils, S., Sauvageot, N., Mazé, A., Laplace, J.-M., Auffray, Y., Deutscher, J., et al. (2007). The cold shock response of Lactobacillus casei: relation between HPr phosphorylation and resistance to freeze/thaw cycles. J. Mol. Microbiol. Biotechnol. 13, 65-75. doi: 10.1159/000103598.
4. Bouvier, J., Bordes, P., Romeo, Y., Fourçans, A., Bouvier, I., Gutierrez, C., et al. (2000). Characterization of OpuA, a glycine-betaine uptake system of Lactococcus lactis. J. Mol. Microbiol. Biotechnol. 2, 199-205. Available online at: https://www.caister.com/jmmb/tocs/v2n2toc.html.
5. Bove, P., Capozzi, V., Garofalo, C., Rieu, A., Spano, G., Fiocco, D. (2012). Inactivation of the ftsH gene of Lactobacillus plantarum WCFS1: effects on growth, stress tolerance, cell surface properties and biofilm formation. Microbiol. Res. 167, 187-193. doi: 10.1016/j.micres.2011.07.001.
6. Broadbent, J. R., Larsen, R. L., Deibel, V., Steele, J. L. (2010). Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid Stress. J. Bacteriol. 192, 2445-2458. doi: 10.1128/JB.01618-09.
7. Bron, P. A., Molenaar, D., de Vos, W. M., Kleerebezem, M. (2006). DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. J. Appl. Microbiol. 100, 728-738. doi: 10.1111/j.1365-2672.2006.02891.x.
8. Burns, P., Sanchez, B., Vinderola, G., Ruas-Madiedo, P., Ruiz, L., Margolles, A., et al. (2010). Inside the adaptation process of Lactobacillus delbrueckii subsp. lactis to bile. Int. J. Food Microbiol. 142, 132-141. doi: 10.1016/j.ijfoodmicro.2010.06.013.
9. Cai, H., Thompson, R., Budinich, M. F., Broadbent, J. R., Steele, J. L. (2010). Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol. Evol. 1, 239-257. doi: 10.1093/gbe/evp019.
10. Cotter, P. D., Hill, C. (2003). Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67, 429-453. doi: 10.1128/MMBR.67.3.429-453.2003.
11. De Angelis, M., Gobbetti, M. (2004). Environmental stress responses in Lactobacillus: a review. Proteomics 4, 106-122. doi: 10.1002/pmic.200300497.
12. de Roos, N. M., Katan, M. B. (2000). Effects of probiotic bacteria on diarrhea, lipid metabolism and carcinogenesis: a review of papers published between 1988 and 1998. Am. J. Clin. Nutr. 71, 405-411. doi: 10.1093/ajcn/71.2.405.
13. Detmers, F. J., Lanfermeijer, F. C., Poolman, B. (2001). Peptides and ATP binding cassette peptide transporters. Res. Microbiol. 152, 245-258. doi: 10.1016/S0923-2508(01)01196-2.
14. Douillard, F. P., Ribbera, A., Jarvinen, H. M., Kant, R., Pietila, T. E., Randazzo, C., et al. (2013). Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics. Appl. Environ. Microbiol. 79, 1923-1933. doi: 10.1128/AEM.03467-12.
15. Duar, R. M., Lin, X. B., Zheng, J., Martino, M. E., Grenier, T., Pérez-Muñoz, M. E., et al. (2017). Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol. Rev. 41, S27-S48. doi: 10.1093/femsre/fux030.
16. Gury, J., Seraut, H., Tran, N. P., Barthelmebs, L., Weidmann, S., Gervais, P., et al. (2009). Inactivation of PadR, the repressor of the phenolic acid stress response, by molecular interaction with Usp1, a universal stress protein from Lactobacillus plantarum, in Escherichia coli. Appl. Environ. Microbiol. 75, 5273-5283. doi: 10.1128/AEM.00774-09.
17. Hamon, E., Horvatovich, P., Bisch, M., Bringel, F., Marchioni, E., Aoudé-Werner, D., et al. (2012). Investigation of biomarkers of bile tolerance in Lactobacillus casei using comparative proteomics. J. Proteome Res. 11, 109-118. doi: 10.1021/pr200828t.
18. Hamon, E., Horvatovich, P., Izquierdo, E., Bringel, F., Marchioni, E., Aoudé-Werner, D., et al. (2011). Comparative proteomic analysis of Lactobacillus plantarum for the identification of key proteins in bile tolerance. BMC Microbiol. 11:63. doi: 10.1186/1471-2180-11-63.
19. Hannig, C., Hannig, M., Rehmer, O., Braun, G., Hellwig, E., Al-Ahmad, A. (2007). Fluorescence microscopic visualization and quantification of initial bacterial colonization on enamel in situ. Arch. Oral Biol. 52, 1048-1056. doi: 10.1016/j.archoralbio.2007.05.006.
20. Hosseini Nezhad, M., Hussain, M. A., Britz, M. L. (2015). Stress Responses in Probiotic Lactobacillus casei. Crit. Rev. Food Sci. Nutr. 55, 740-749. doi: 10.1080/10408398.2012.675601.
21. Ingrassia, I., Leplingard, A., Darfeuille-Michaud, A. (2005). Lactobacillus casei DN-114 001 inhibits the ability of adherent-invasive Escherichia coli isolated from Crohn's disease patients to adhere to and to invade intestinal epithelial cells. Appl. Environ. Microbiol. 71, 2880-2887. doi: 10.1128/AEM.71.6.2880-2887.2005.
22. Judicial Commission of the International Committee on Systematics of Bacteria (2008). The type strain of Lactobacillus casei is ATCC 393, ATCC 334 cannot serve as the type because it represents a different taxon, the name Lactobacillus paracasei and its subspecies names are not rejected and the revival of the name "Lactobacillus zeae" contravenes Rules 51b (1) and (2) of the International Code of Nomenclature of Bacteria. Opinion 82. Int. J. Syst. Evol. Microbiol. 58, 1764-1765. doi: 10.1099/ijs.0.2008/005330-0.
23. Koskenniemi, K., Laakso, K., Koponen, J., Kankainen, M., Greco, D., Auvinen, P., et al. (2011). Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG. Mol. Cell. Proteomics 10:M110.002741. doi: 10.1074/mcp.M110.002741.
24. Kvint, K., Nachin, L., Diez, A., Nyström, T. (2003). The bacterial universal stress protein: function and regulation. Curr. Opin. Microbiol. 6, 140-145. doi: 10.1016/S1369-5274(03)00025-0.
25. Licandro-Seraut, H., Brinster, S., van de Guchte, M., Scornec, H., Maguin, E., Sansonetti, P., et al. (2012). Development of an efficient in vivo system (Pjunc-TpaseIS1223) for random transposon mutagenesis of Lactobacillus casei. Appl. Environ. Microbiol. 78, 5417-5423. doi: 10.1128/AEM.00531-12.
26. Licandro-Seraut, H., Gury, J., Tran, N. P., Barthelmebs, L., Cavin, J. F. (2008). Kinetics and intensity of the expression of genes involved in the stress response tightly induced by phenolic acids in Lactobacillus plantarum. J. Mol. Microbiol. Biotechnol. 14, 41-47. doi: 10.1159/000106081.
27. Licandro-Seraut, H., Scornec, H., Pédron, T., Cavin, J.-F., Sansonetti, P. J. (2014). Functional genomics of Lactobacillus casei establishment in the gut. Proc. Natl. Acad. Sci. U.S.A. 111, E3101-E3109. doi: 10.1073/pnas.1411883111.
28. Livak, K. J., Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262.
29. Munoz-Provencio, D., Rodriguez-Diaz, J., Collado, M. C., Langella, P., Bermudez-Humaran, L. G., Monedero, V. (2012). Functional analysis of the Lactobacillus casei BL23 sortases. Appl. Environ. Microbiol. 78, 8684-8693. doi: 10.1128/AEM.02287-12.
30. Papadimitriou, K., Alegría, á., Bron, P. A., de Angelis, M., Gobbetti, M., Kleerebezem, M., et al. (2016). Stress physiology of lactic acid bacteria. Microbiol. Mol. Biol. Rev. 80, 837-890. doi: 10.1128/MMBR.00076-15.
31. Papadimitriou, K., Zoumpopoulou, G., Foligné, B., Alexandraki, V., Kazou, M., Pot, B., et al. (2015). Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front. Microbiol. 6:58. doi: 10.3389/fmicb.2015.00058.
32. Perpetuini, G., Pham-Hoang, B. N., Scornec, H., Tofalo, R., Schirone, M., Suzzi, G., et al. (2016). In Lactobacillus pentosus, the olive brine adaptation genes are required for biofilm formation. Int. J. Food Microbiol. 216, 104-109. doi: 10.1016/j.ijfoodmicro.2015.10.002.
33. Perpetuini, G., Scornec, H., Tofalo, R., Serror, P., Schirone, M., Suzzi, G., et al. (2013). Identification of critical genes for growth in olive brine by transposon mutagenesis of Lactobacillus pentosus C11. Appl. Environ. Microbiol. 79, 4568-4575. doi: 10.1128/AEM.01159-13.
34. Price, M. N., Deutschbauer, A. M., Skerker, J. M., Wetmore, K. M., Ruths, T., Mar, J. S., et al. (2013). Indirect and suboptimal control of gene expression is widespread in bacteria. Mol. Syst. Biol. 9:660. doi: 10.1038/msb.2013.16.
35. Saxelin, M., Tynkkynen, S., Mattila-Sandholm, T., de Vos, W. M. (2005). Probiotic and other functional microbes: from markets to mechanisms. Curr. Opin. Biotechnol. 16, 204-211. doi: 10.1016/j.copbio.2005.02.003.
36. Scornec, H., Tichit, M., Bouchier, C., Pédron, T., Cavin, J.-F., Sansonetti, P. J., et al. (2014). Rapid 96-well plates DNA extraction and sequencing procedures to identify genome-wide transposon insertion sites in a difficult to lyse bacterium: Lactobacillus casei. J. Microbiol. Methods 106, 78-82. doi: 10.1016/j.mimet.2014.08.001.
37. Smokvina, T., Wels, M., Polka, J., Chervaux, C., Brisse, S., Boekhorst, J., et al. (2013). Lactobacillus paracasei comparative genomics: towards species pan-genome definition and exploitation of diversity. PLoS ONE 8:e68731. doi: 10.1371/journal.pone.0068731.
38. Stevens, M. J. A., Molenaar, D., de Jong, A., de Vos, W. M., Kleerebezem, M. (2010). Involvement of the mannose phosphotransferase system of Lactobacillus plantarum WCFS1 in peroxide stress tolerance. Appl. Environ. Microbiol. 76, 3748-3752. doi: 10.1128/AEM.00073-10.
39. Sugimoto, S., Abdullah-Al-Mahin Sonomoto, K. (2008). Molecular chaperones in lactic acid bacteria: physiological consequences and biochemical properties. J. Biosci. Bioeng. 106, 324-336. doi: 10.1263/jbb.106.324.
40. Tawakoli, P. N., Al-Ahmad, A., Hoth-Hannig, W., Hannig, M., Hannig, C. (2013). Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm. Clin. Oral Invest. 17, 841-850. doi: 10.1007/s00784-012-0792-3.
41. Tong, Y., Zhai, Q., Lu, W., Tian, F., Zhao, J., Zhang, H., et al. (2017). New insights in integrated response mechanism of Lactobacillus plantarum under excessive manganese stress. Food Res. Int. 102, 323-332. doi: 10.1016/j.foodres.2017.10.014.
42. Tran, N. P., Gury, J., Dartois, V., Nguyen, T. K. C., Seraut, H., Barthelmebs, L., et al. (2008). Phenolic acid-mediated regulation of the padC gene, encoding the phenolic acid decarboxylase of Bacillus subtilis. J. Bacteriol. 190, 3213-3224. doi: 10.1128/JB.01936-07.
43. Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., Leunissen, J. A. M. (2007). Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35, W71-W74. doi: 10.1093/nar/gkm306.
44. van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S. D., Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82, 187-216. doi: 10.1023/A:1020631532202.
45. Wang, G., Li, D., Ma, X., An, H., Zhai, Z., Ren, F., et al. (2015). Functional role of oppA encoding an oligopeptide-binding protein from Lactobacillus salivarius Ren in bile tolerance. J. Ind. Microbiol. Biotechnol. 42, 1167-1174. doi: 10.1007/s10295-015-1634-5.
46. Wu, C., Zhang, J., Chen, W., Wang, M., Du, G., Chen, J. (2012). A combined physiological and proteomic approach to reveal lactic-acid-induced alterations in Lactobacillus casei Zhang and its mutant with enhanced lactic acid tolerance. Appl. Microbiol. Biotechnol. 93, 707-722. doi: 10.1007/s00253-011-3757-6.
47. Wu, R., Sun, Z., Wu, J., Meng, H., Zhang, H. (2010). Effect of bile salts stress on protein synthesis of Lactobacillus casei Zhang revealed by 2-dimensional gel electrophoresis. J. Dairy Sci. 93, 3858-3868. doi: 10.3168/jds.2009-2967.
48. Xie, Y., Chou, L., Cutler, A., Weimer, B. (2004). DNA Macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl. Environ. Microbiol. 70, 6738-6747. doi: 10.1128/AEM.70.11.6738-6747.2004.
49. Yamasaki-Yashiki, S., Sawada, H., Kino-oka, M., Katakura, Y. (2017). Analysis of gene expression profiles of Lactobacillus paracasei induced by direct contact with Saccharomyces cerevisiae through recognition of yeast mannan. Biosci. Microbiota Food Health 36, 17-25. doi: 10.12938/bmfh.BMFH-2016-015.
50. Zotta, T., Guidone, A., Tremonte, P., Parente, E., Ricciardi, A. (2012). A comparison of fluorescent stains for the assessment of viability and metabolic activity of lactic acid bacteria. World J. Microbiol. Biotechnol. 28, 919-927. doi: 10.1007/s11274-011-0889-x.