Gene replacement and fluorescent labeling to study the functional role of exopolysaccharides in Bifidobacterium animalis subsp. lactis

Frontiers in Microbiology

Volumn 8, Issue JUL, 2017, Pages

  Castro Bravo, Nuria ^a   Hidalgo Cantabrana, Claudio ^a   Rodriguez Carvajal, Miguel A ^b   Ruas Madiedo, Patricia ^a   Margolles, Abelardo ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Bifidobacterium; Biofilms; Exopolysaccharide; Fluorescent proteins; Gene replacement; NMR; SEC MALS

Indexed keywords

EXOPOLYSACCHARIDE; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN;

ARTICLE; BACTERIAL GENETICS; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS; BIOFILM; CELL ADHESION; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE REPLACEMENT THERAPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSICAL CHEMISTRY; POLYMERASE CHAIN REACTION; PROTON NUCLEAR MAGNETIC RESONANCE;

EID: 85026418423     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01405     Document Type: Article

References (49)

1. Alvarez-Martín, P., Flórez, A. B., Margolles, A., del Solar, G., and Mayo, B. (2008). Improved cloning vectors for bifidobacteria, based on the Bifidobacterium catenulatum pBC1 replicon. Appl. Environ. Microbiol. 74, 4656-4665. doi: 10.1128/AEM.00074-08.
2. Arigoni, F., and Delley, M. (2008). Genetic remodeling in Bifidobacterium. International patent WO 2008019886 A1. Washington, DC: U.S. Patent and Trademark Office.
3. Bogsan, C. S. B., Ferreira, L., Maldonado, C., Perdigon, G., Almeida, S. R., and Oliveira, M. N. (2014). Fermented or unfermented milk using Bifidobacterium animalis subsp. lactis HN019: technological approach determines the probiotic modulation of mucosal cellular immunity. Food Res. Int. 64, 283-288.
4. Chen, X. Y., Woodward, A., Zijlstra, R. T., and Gänzle, M. G. (2014). Exopolysaccharides synthesized by Lactobacillus reuteri protect against enterotoxigenic Escherichia coli in Piglets. Appl. Environ. Microbiol. 80, 5752-5760. doi: 10.1128/AEM.01782-14.
5. Cronin, M., Sleator, R. D., Hill, C., Fitzgerald, G. F., and van Sinderen, D. (2008). Development of a luciferase-based reporter system to monitor Bifidobacterium breve UCC2003 persistence in mice. BMC Microbiol. 8:161. doi: 10.1186/1471-2180-8-161.
6. Dertli, E., Mayer, M. J., and Narbad, A. (2015). Impact of the exopolysaccharide layer on biofilms, adhesion and resistance to stress in Lactobacillus johnsonii FI9785. BMC Microbiol. 15:8. doi: 10.1186/s12866-015-0347-2.
7. Fanning, S., Hall, L. J., Cronin, M., Zomer, A., MacSharry, J., Goulding, D., et al. (2012). Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc. Natl. Acad. Sci. U.S.A. 109, 2108-2113. doi: 10.1073/pnas.1115621109.
8. Ferrario, C., Milani, C., Mancabelli, L., Lugli, G. A., Duranti, S., Mangifesta, M., et al. (2016). Modulation of the eps-ome transcription of bifidobacteria through simulation of human intestinal environment. FEMS Microbiol. Ecol. 92:fiw056. doi: 10.1093/femsec/fiw056.
9. Food, and Agricultural Organization of the United Nations, and World Health Organization [FAO/WHO] (2002). Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. Rome: FAO.
10. Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., et al. (2011). Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-547. doi: 10.1038/nature09646.
11. Gareau, M. G., Sherman, P. M., and Walker, W. A. (2010). Probiotics and the gut microbiota in intestinal health and disease. Nat. Rev. Gastroenterol. Hepatol. 7, 503-514. doi: 10.1038/nrgastro.2010.117.
12. Gottlieb, H. E., Kotlyar, V., and Nudelman, A. (1997). NMR chemical shifts of common laboratory solvents as trace impurities. J. Org. Chem. 62, 7512-7515.
13. Grimm, V., Gleinser, M., Neu, C., Zhurina, D., and Riedel, C. H. (2014). Expression of fluorescent proteins in bifidobacteria for analysis of host-microbe interactions. Appl. Environ. Microbiol. 80, 2842-2850. doi: 10.1128/AEM.04261-13.
14. Gutiérrez, D., Hidalgo-Cantabrana, C., Rodríguez, A., García, P., and Ruas-Madiedo, P. (2016). Monitoring in real time the formation and removal of biofilms from clinical related pathogens using an impedance-based technology. PLoS ONE 11:e0163966. doi: 10.1371/journal.pone.0163966.
15. Hidalgo-Cantabrana, C., Algieri, F., Rodriguez-Nogales, A., Vezza, T., Martínez-Camblor, P., Margolles, A., et al. (2016). Effect of a ropy exopolysaccharide-producing Bifidobacterium animalis subsp. lactis strain orally administered on DSS-induced colitis mice model. Front. Microbiol. 7:868. doi: 10.3389/fmicb.2016.00868.
16. Hidalgo-Cantabrana, C., Sánchez, B., álvarez-Martín, P., López, P., Martínez-álvarez, N., Delley, M., et al. (2015). A single mutation in the gene responsible for the mucoid phenotype of Bifidobacterium animalis subsp. lactis confers surface and functional characteristics. Appl. Environ. Microbiol. 81, 7960-7968. doi: 10.1128/AEM.02095-15.
17. Hidalgo-Cantabrana, C., Sánchez, B., Milani, C., Ventura, M., Margolles, A., and Ruas-Madiedo, P. (2014). Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Appl. Environ. Microbiol. 80, 9-18. doi: 10.1128/AEM.02977-13.
18. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., et al. (2014). 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.
19. Hirayama, Y., Sakanaka, M., Fukuma, H., Murayama, H., Kano, Y., Fukiya, S., et al. (2012). Development of a double-crossover markerless gene deletion system in Bifidobacterium longum: functional analysis of the-galactosidase gene for raffinose assimilation. Appl. Environ. Microbiol. 78, 4984-4994. doi: 10.1128/AEM.00588-12.
20. Horn, N., Wegmann, U., Dertli, E., Mulholland, F., Collins, S. R. A., Waldron, K. W., et al. (2014). Spontaneous mutation reveals influence of exopolysaccharide on Lactobacillus johnsonii surface characteristics. PLoS ONE 8:e59957. doi: 10.1371/journal.pone.0059957.
21. Ksonzeková, P., Bystricky, P., Vlcková, S., Pätoprsty, V., Pulzová, L., Mudronová, D., et al. (2016). Exopolysaccharides of Lactobacillus reuteri: their influence ona dherence of E. coli to epithelial cells and inflammatory response. Carbohydr. Polym. 141, 10-19. doi: 10.1016/j.carbpol.2015.12.037.
22. Landete, J. M., Medina, M., and Arqués, J. L. (2016). Fluorescent reporter systems for tracking probiotic lactic acid bacteria and bifidobacteria. World J. Microbiol. Biotechnol. 32, 119. doi: 10.1007/s11274-016-2077-5.
23. Landete, J. M., Peirotén,á, Rodríguez, E., Margolles, A., Medina, M., and Arqués, J. L. (2014). Anaerobic green fluorescent protein as a marker of Bifidobacterium strains. Int. J. Food Microbiol. 175, 6-13. doi: 10.1016/j.ijfoodmicro.2014.01.008.
24. Lebeer, S., Claes, I., Tytgat, H. L. P., Verhoeven, T. L. A., Marien, E., von Ossowski, I., et al. (2012). Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 78, 185-193. doi: 10.1128/AEM.06192-11.
25. Lebeer, S., Claes, I. J. J., Verhoeven, T. L. A., Vanderleyden, J., and De Keersmaecker, S. C. J. (2010a). Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb. Biotechnol. 4, 368-374. doi: 10.1111/j.1751-7915.2010.00199.x.
26. Lebeer, S., Vanderleyden, J., and De Keersmaecker, S. C. J. (2010b). Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171-184. doi: 10.1038/nrmicro2297.
27. Lebeer, S., Verhoeven, T. L. A., Francius, G., Schoofs, G., Lambrichts, I., Dufrêne, Y., et al. (2009). Identification of a gene Cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl. Environ. Microbiol. 75, 3554-3563. doi: 10.1128/AEM.02919-08.
28. Leivers, S., Hidalgo-Cantabrana, C., Robinson, G., Margolles, A., Ruas-Madiedo, P., and Laws, A. P. (2011). Structure of the high molecular weight exopolysaccharide produced by Bifidobacterium animalis subsp.lactis IPLA-R1 and sequence analysis of its putative eps cluster. Carbohyd. Res. 346, 2710-2717. doi: 10.1016/j.carres.2011.09.010.
29. López, P., Monteserín, D. C., Gueimonde, M., de los Reyes-Gavilán, C. G., Margolles, A., Suárez, A., et al. (2012). Exopolysaccharide-producing Bifidobacterium strains elicit different in vitro responses upon interaction with human cells. Food Res. Int. 46, 99-107.
30. Meira, Q. G. S., de Medeiros Barbosa, I., Alves Aguiar Athayde, A. J., de Siqueira-Junior, J. P., and de Souza, E. L. (2012). Influence of temperature and surface kind on biofilm formation by Staphylococcus aureus from food-contact surfaces and sensitivity to sanitizers. Food Control 25, 469-475.
31. Montenegro-Rodríguez, C., Peirotén, A., Sanchez-Jimenez, A., Arqués, J. L., and Landete, J. M. (2015). Analysis of gene expression of bifidobacteria using as the reporter an anaerobic fluorescent protein. Biotechnol. Lett. 37, 1405-1413. doi: 10.1007/s10529-015-1802-8.
32. Nácher-Vázquez, M., Ballesteros, N., Canales, A., Rodríguez Saint-Jean, S., Pérez-Prieto, S. I., Prieto, A., et al. (2015). Dextrans produced by lactic acid bacteria exhibit antiviral and immunomodulatory activity against salmonid viruses. Carbohydr. Polym. 124, 292-301. doi: 10.1016/j.carbpol.2015.02.020.
33. Nikolic, M., López, P., Strahinic, I., Suárez, A., Kojic, M., Fernández-García, M., et al. (2012). Characterisation of the exopolysaccharide (EPS)-producing Lactobacillus paraplantarum BGCG11 and its non-EPS producing derivative strains as potential probiotics. Int. J. Food Microbiol. 158, 155-162. doi: 10.1016/j.ijfoodmicro.2012.07.015.
34. O'Toole, P. W., Marchesi, J. R., and Hill, C. (2017). Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nature Microbiol. 2, 17057. doi: 10.1038/nmicrobiol.2017.57.
35. Reid, G., Younes, J. A., Van der Mei, H. C., Gloor, G. B., Knight, R., and Busscher, H. J. (2011). Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat. Rev. Microbiol. 9, 27-38. doi: 10.1038/nrmicro2473.
36. Rossi, O., Khan, M. T., Schwarzer, M., Hudcovic, T., Srutkova, D., Duncan, S. H., et al. (2015). Faecalibacterium prausnitzii strain HTF-F and its extracellular pPolymeric matrix attenuate clinical parameters in DSS-induced colitis. PLoS ONE 10:e0123013. doi: 10.1371/journal.pone.0123013.
37. Ruas-Madiedo, P., Gueimonde, M., Margolles, A., de los Reyes-Gavilán, C. G., and Salminen, S. (2006). Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J. Food Proct. 69, 2011-2015.
38. Ruas-Madiedo, P., Medrano, M., Salazar, N., de los Reyes-Gavilán, C. G., Pérez, P. F., and Abraham, A. G. (2010). Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J. Appl. Microbiol. 109, 2079-2086. doi: 10.1111/j.1365-2672.2010.04839.x.
39. Ruiz, L., O'Connell-Motherway, M., Zomer, A., de los Reyes-Gavilán, C. G., Margolles, A., and van Sinderen, D. (2012). A bile-inducible membrane protein mediates bifidobacterial bile resistance. Microb. Biotechnol. 5, 523-535. doi: 10.1111/j.1751-7915.2011.00329.x.
40. Sánchez, B., Champomier-Vergès, M. C., Anglade, P., Baraige, F., de Los Reyes-Gavilán, C. G., Margolles, A., et al. (2005). Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J. Bacteriol. 187, 5799-5808.
41. Sánchez, B., Champomier-Vergès, M. C., Collado, M. D. C., Anglade, P., Baraige, F., Sanz, Y., et al. (2007). Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl. Environ. Microbiol. 73, 6450-6459.
42. Schiavi, E., Gleinser, M., Molloy, E., Groeger, F., Frei, R., Ferstl, R., et al. (2016). The surface-associated exopolysaccharide of Bifidobacterium longum 35624 plays an essential role in dampening host proinflammatory responses and repressing local TH17 responses. Appl. Environ. Microbiol. 82, 7185-7196.
43. Tojo, R., Suárez, A., Clemente, M. G., de los Reyes-Gavilán, C. G., Margolles, A., Gueimonde, M., et al. (2014). Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 20, 15163-15176. doi: 10.3748/wjg.v20.i41.15163.
44. Uemura, Y., and Matsumoto, M. (2014). Chemical structure of the cell wall-associated polysaccharide of Bifidobacterium animalis subsp. lactis LKM512. Glycoconjugate J. 31, 555-561. doi: 10.1007/s10719-014-9534-x.
45. Vallejo, A. N., Pogulis, R. J., and Pease, L. R. (1994). In vitro synthesis of novel genes: mutagenesis and recombination by PCR. Genome Res. 4, S123-S130.
46. Wan, L. Y. M., Chen, Z. J., Shah, N. P., and El-Nezami, H. (2015). Modulation of intestinal epithelial defense responses by probiotic bacteria. Crit. Rev. Food Sci. Nutr. 56, 2628-2641. doi: 10.1080/10408398.2014.905450.
47. Wei, X., Wang, S., Zhao, X., Wang, X., Li, H., Lin, W., et al. (2016). Proteomic profiling of Bifidobacterium bifidum S17 cultivated under in vitro conditions. Front. Microbiol. 7:97. doi: 10.3389/fmicb.2016.00097.
48. Westermann, C., Gleinser, M., Corr, S. C., and Riedel, C. U. (2016). A critical evaluation of bifidobacterial adhesion to the host tissue. Front. Microbiol. 7:1220. doi: 10.3389/fmicb.2016.01220.
49. Zivkovic, M., Miljkovi, M. S., Ruas-Madiedo, P., Markeli, M. B., Veljovic, K., Tolinacki, M., et al. (2016). EPS-SJ exopolysaccharide produced by the strain Lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E.coli association to Caco-2 cells. Front. Microbiol. 7:286. doi: 10.3389/fmicb.2016.00286.