A Critical Evaluation of Bifidobacterial Adhesion to the Host Tissue

Christina Westermann, Marita Gleinser, Sinéad C Corr, Christian U Riedel, Christina Westermann, Marita Gleinser, Sinéad C Corr, Christian U Riedel

Abstract

Bifidobacteria are common inhabitants of the human gastrointestinal tract that, despite a long history of research, have not shown any pathogenic potential whatsoever. By contrast, some bifidobacteria are associated with a number of health-related benefits for the host. The reported beneficial effects of bifidobacteria include competitive exclusion of pathogens, alleviation of symptoms of irritable bowel syndrome and inflammatory bowel disease, and modulation of intestinal and systemic immune responses. Based on these effects, bifidobacteria are widely used as probiotics by pharmaceutical and dairy industries. In order to exert a beneficial effect bifidobacteria have to, at least transiently, colonize the host in a sufficient population size. Besides other criteria such as resistance to manufacturing processes and intestinal transit, potential probiotic bacteria are tested for adhesion to the host structures including intestinal epithelial cells, mucus, and extracellular matrix components. In the present review article, we summarize the current knowledge on bifidobacterial structures that mediate adhesion to host tissue and compare these to similar structures of pathogenic bacteria. This reveals that most of the adhesive structures and mechanisms involved in adhesion of bifidobacteria to host tissue are similar or even identical to those employed by pathogens to cause disease. It is thus reasonable to assume that these structures and mechanisms are equally important for commensal or probiotic bacteria and play a similar role in the beneficial effects exerted by bifidobacteria.

Keywords: Bifidobacterium; adhesion; host interaction; probiotic.

References

    1. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D. R., et al. (2011). Enterotypes of the human gut microbiome. Nature 473 174–180. 10.1038/nature09944
    1. Bäckhed F., Roswall J., Peng Y., Feng Q., Jia H., Kovatcheva-Datchary P., et al. (2015). Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17 690–703. 10.1016/j.chom.2015.04.004
    1. Bermudez-Brito M., Plaza-Díaz J., Muñoz-Quezada S., Gómez-Llorente C., Gil A. (2012). Probiotic mechanisms of action. Ann. Nutr. Metab. 61 160–174. 10.1159/000342079
    1. Bernet M. F., Brassart D., Neeser J. R., Servin A. L. (1993). Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl. Environ. Microbiol. 59 4121–4128.
    1. Bhavsar A. P., Guttman J. A., Finlay B. B. (2007). Manipulation of host-cell pathways by bacterial pathogens. Nature 449 827–834. 10.1038/nature06247
    1. Bottacini F., O Connell Motherway M., Kuczynski J., O Connell K. J., Serafini F., Duranti S., et al. (2014). Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics 15:170 10.1186/1471-2164-15-170
    1. Brook I., Myhal M. L. (1991). Adherence of Bacteroides fragilis group species. Infect. Immun. 59 742–744.
    1. Buffie C. G., Pamer E. G. (2013). Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13 790–801. 10.1038/nri3535
    1. Candela M., Bergmann S., Vici M., Vitali B., Turroni S., Eikmanns B. J., et al. (2007). Binding of human plasminogen to Bifidobacterium. J. Bacteriol. 189 5929–5936. 10.1128/JB.00159-07
    1. Candela M., Biagi E., Centanni M., Turroni S., Vici M., Musiani F., et al. (2009). Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 155 3294–3303. 10.1099/mic.0.028795-0
    1. Candela M., Centanni M., Fiori J., Biagi E., Turroni S., Orrico C., et al. (2010). DnaK from Bifidobacterium animalis subsp. lactis is a surface-exposed human plasminogen receptor upregulated in response to bile salts. Microbiology 156 1609–1618. 10.1099/mic.0.038307-0
    1. Candela M., Perna F., Carnevali P., Vitali B., Ciati R., Gionchetti P., et al. (2008). Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int. J. Food Microbiol. 125 286–292. 10.1016/j.ijfoodmicro.2008.04.012
    1. Colagiorgi A., Turroni F., Mancabelli L., Serafini F., Secchi A., van Sinderen D., et al. (2015). Insights into teichoic acid biosynthesis by Bifidobacterium bifidum PRL2010. FEMS Microbiol. Lett. 362:fnv141 10.1093/femsle/fnv141
    1. Collado M. C., Gueimonde M., Hernández M., Sanz Y., Salminen S. (2005). Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J. Food Prot. 68 2672–2678.
    1. de O Ferreira E., Araújo Lobo L., Barreiros Petrópolis D., dos S Avelar K. E., Ferreira M. C., e Silva Filho F. C., et al. (2006). A Bacteroides fragilis surface glycoprotein mediates the interaction between the bacterium and the extracellular matrix component laminin-1. Res. Microbiol. 157 960–966. 10.1016/j.resmic.2006.09.005
    1. Del Re B., Sgorbati B., Miglioli M., Palenzona D. (2000). Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett. Appl. Microbiol. 31 438–442. 10.1046/j.1365-2672.2000.00845.x
    1. Duranti S., Milani C., Lugli G. A., Turroni F., Mancabelli L., Sanchez B., et al. (2015). Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ. Microbiol. 17 2515–2531. 10.1111/1462-2920.12743
    1. Duranti S., Turroni F., Lugli G. A., Milani C., Viappiani A., Mangifesta M., et al. (2014). Genomic characterization and transcriptional studies of the starch-utilizing Bifidobacterium adolescentis 22L. Appl. Environ. Microbiol. 80 6080–6090. 10.1128/AEM.01993-14
    1. Fernández L., Langa S., Martín V., Maldonado A., Jiménez E., Martín R., et al. (2013). The human milk microbiota: origin and potential roles in health and disease. Pharmacol. Res. 69 1–10. 10.1016/j.phrs.2012.09.001
    1. Ferreira E. O., Falcão L. S., Vallim D. C., Santos F. J., Andrade J. R. C., Andrade A. F. B., et al. (2002). Bacteroides fragilis adherence to Caco-2 cells. Anaerobe 8 307–314. 10.1016/S1075-9964(03)00008-8
    1. Ferreira Ede O., Teixeira F. L., Cordeiro F., Araujo Lobo L., Rocha E. R., Smith J. C., et al. (2013). The Bfp60 surface adhesin is an extracellular matrix and plasminogen protein interacting in Bacteroides fragilis. Int. J. Med. Microbiol. 303 492–497. 10.1016/j.ijmm.2013.06.007
    1. Foligné B., Daniel C., Pot B. (2013). Probiotics from research to market: the possibilities, risks and challenges. Curr. Opin. Microbiol. 16 284–292. 10.1016/j.mib.2013.06.008
    1. Foroni E., Serafini F., Amidani D., Turroni F., He F., Bottacini F., et al. (2011). Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb. Cell Fact. 10(Suppl. 1) S16 10.1186/1475-2859-10-S1-S16
    1. Gareau M. G., Sherman P. M., Walker W. A. (2010). Probiotics and the gut microbiota in intestinal health and disease. Nat. Rev. Gastroenterol. Hepatol. 7 503–514. 10.1038/nrgastro.2010.117
    1. Gilad O., Svensson B., Viborg A. H., Stuer-Lauridsen B., Jacobsen S. (2011). The extracellular proteome of Bifidobacterium animalis subsp. lactis BB-12 reveals proteins with putative roles in probiotic effects. Proteomics 11 2503–2514. 10.1002/pmic.201000716
    1. Gleinser M., Grimm V., Zhurina D., Yuan J., Riedel C. U. (2012). Improved adhesive properties of recombinant bifidobacteria expressing the Bifidobacterium bifidum-specific lipoprotein BopA. Microb. Cell Fact. 11 80 10.1186/1475-2859-11-80
    1. González-Rodríguez I., Sánchez B., Ruiz L., Turroni F., Ventura M., Ruas-Madiedo P., et al. (2012). Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl. Environ. Microbiol. 78 3992–3998. 10.1128/AEM.08024-11
    1. Grimm V., Gleinser M., Neu C., Zhurina D., Riedel C. U. (2014). Expression of fluorescent proteins in bifidobacteria for analysis of host-microbe interactions. Appl. Environ. Microbiol. 80 2842–2850. 10.1128/AEM.04261-13
    1. Grönlund M.-M., Grześkowiak L., Isolauri E., Salminen S. (2011). Influence of mother’s intestinal microbiota on gut colonization in the infant. Gut Microbes 2 227–233. 10.4161/gmic.2.4.16799
    1. Guglielmetti S., Tamagnini I., Minuzzo M., Arioli S., Parini C., Comelli E., et al. (2009). Study of the adhesion of Bifidobacterium bifidum MIMBb75 to human intestinal cell lines. Curr. Microbiol. 59 167–172. 10.1007/s00284-009-9415-x
    1. Guglielmetti S., Tamagnini I., Mora D., Minuzzo M., Scarafoni A., Arioli S., et al. (2008). Implication of an outer surface lipoprotein in adhesion of Bifidobacterium bifidum to Caco-2 cells. Appl. Environ. Microbiol. 74 4695–4702. 10.1128/AEM.00124-08
    1. Guglielmetti S., Taverniti V., Minuzzo M., Arioli S., Zanoni I., Stuknyte M., et al. (2010). A dairy bacterium displays in vitro probiotic properties for the pharyngeal mucosa by antagonizing group A streptococci and modulating the immune response. Infect. Immun. 78 4734–4743. 10.1128/IAI.00559-10
    1. He F., Ouwehan A. C., Hashimoto H., Isolauri E., Benno Y., Salminen S. (2001). Adhesion of Bifidobacterium spp. to human intestinal mucus. Microbiol. Immunol. 45 259–262. 10.1111/j.1348-0421.2001.tb02615.x
    1. Henderson B. (2014). An overview of protein moonlighting in bacterial infection. Biochem. Soc. Trans. 42 1720–1727. 10.1042/BST20140236
    1. Henderson B., Martin A. (2011). Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect. Immun. 79 3476–3491. 10.1128/IAI.00179-11
    1. Hidalgo-Cantabrana C., Sánchez B., Milani C., Ventura M., Margolles A., Ruas-Madiedo P. (2014). Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Appl. Environ. Microbiol. 80 9–18. 10.1128/AEM.02977-13
    1. Hirt H., Erlandsen S. L., Dunny G. M. (2000). Heterologous inducible expression of Enterococcus faecalis pCF10 aggregation substance asc10 in Lactococcus lactis and Streptococcus gordonii contributes to cell hydrophobicity and adhesion to fibrin. J. Bacteriol. 182 2299–2306. 10.1128/JB.182.8.2299-2306.2000
    1. Holmes E., Kinross J., Gibson G. R., Burcelin R., Jia W., Pettersson S., et al. (2012). Therapeutic modulation of microbiota-host metabolic interactions. Sci. Transl. Med. 4:137rv6 10.1126/scitranslmed.3004244
    1. Huang J. Y., Lee S. M., Mazmanian S. K. (2011). The human commensal Bacteroides fragilis binds intestinal mucin. Anaerobe 17 137–141. 10.1016/j.anaerobe.2011.05.017
    1. Huberts D. H. E. W., van der Klei I. J. (2010). Moonlighting proteins: an intriguing mode of multitasking. Biochim. Biophys. Acta 1803 520–525. 10.1016/j.bbamcr.2010.01.022
    1. Izquierdo E., Medina M., Ennahar S., Marchioni E., Sanz Y. (2008). Resistance to simulated gastrointestinal conditions and adhesion to mucus as probiotic criteria for Bifidobacterium longum strains. Curr. Microbiol. 56 613–618. 10.1007/s00284-008-9135-7
    1. Johansson M. E. V. (2014). Mucus layers in inflammatory bowel disease. Inflamm. Bowel Dis. 20 2124–2131. 10.1097/MIB.0000000000000117
    1. Jost T., Lacroix C., Braegger C., Chassard C. (2015). Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr. Rev. 73 426–437. 10.1093/nutrit/nuu016
    1. Kainulainen V., Reunanen J., Hiippala K., Guglielmetti S., Vesterlund S., Palva A., et al. (2013). BopA has no major role in the adhesion of Bifidobacterium bifidum to intestinal epithelial cells, extracellular matrix proteins and mucus. Appl. Environ. Microbiol. 79 6989–6997. 10.1128/AEM.01993-13
    1. Klaenhammer T. R., Kullen M. J. (1999). Selection and design of probiotics. Int. J. Food Microbiol. 50 45–57. 10.1016/S0168-1605(99)00076-8
    1. Kline K. A., Fälker S., Dahlberg S., Normark S., Henriques-Normark B. (2009). Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5 580–592. 10.1016/j.chom.2009.05.011
    1. Kouidhi B., Zmantar T., Hentati H., Bakhrouf A. (2010). Cell surface hydrophobicity, biofilm formation, adhesives properties and molecular detection of adhesins genes in Staphylococcus aureus associated to dental caries. Microb. Pathog. 49 14–22. 10.1016/j.micpath.2010.03.007
    1. Lawley T. D., Walker A. W. (2013). Intestinal colonization resistance. Immunology 138 1–11. 10.1111/j.1365-2567.2012.03616.x
    1. Liu D., Wang S., Xu B., Guo Y., Zhao J., Liu W., et al. (2011). Proteomics analysis of Bifidobacterium longum NCC2705 growing on glucose, fructose, mannose, xylose, ribose, and galactose. Proteomics 11 2628–2638. 10.1002/pmic.201100035
    1. Macfarlane S., Woodmansey E. J., Macfarlane G. T. (2005). Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl. Environ. Microbiol. 71 7483–7492. 10.1128/AEM.71.11.7483-7492.2005
    1. Maier B., Wong G. C. L. (2015). How bacteria use type IV pili machinery on surfaces. Trends Microbiol. 23 775–788. 10.1016/j.tim.2015.09.002
    1. Marchesi J. R., Adams D. H., Fava F., Hermes G. D. A., Hirschfield G. M., Hold G., et al. (2016). The gut microbiota and host health: a new clinical frontier. Gut 65 330–339. 10.1136/gutjnl-2015-309990
    1. Matamoros S., Gras-Leguen C., Le Vacon F., Potel G., de La Cochetiere M.-F. (2013). Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 21 167–173. 10.1016/j.tim.2012.12.001
    1. Niemann H. H., Schubert W. D., Heinz D. W. (2004). Adhesins and invasins of pathogenic bacteria: a structural view. Microbes Infect. 6 101–112. 10.1016/j.micinf.2003.11.001
    1. O’Connell Motherway M., Zomer A., Leahy S. C., Reunanen J., Bottacini F., Claesson M. J., et al. (2011). Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc. Natl. Acad. Sci. U.S.A. 108 11217–11222. 10.1073/pnas.1105380108
    1. Pan W.-H., Li P.-L., Liu Z. (2006). The correlation between surface hydrophobicity and adherence of Bifidobacterium strains from centenarians’ faeces. Anaerobe 12 148–152. 10.1016/j.anaerobe.2006.03.001
    1. 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 10.3389/fmicb.2015.00058
    1. Pérez P. F., Minnaard Y., Disalvo E. A., De Antoni G. L. (1998). Surface properties of bifidobacterial strains of human origin. Appl. Environ. Microbiol. 64 21–26.
    1. Preising J., Philippe D., Gleinser M., Wei H., Blum S., Eikmanns B. J., et al. (2010). Selection of bifidobacteria based on adhesion and anti-inflammatory capacity in vitro for amelioration of murine colitis. Appl. Environ. Microbiol. 76 3048–3051. 10.1128/AEM.03127-09
    1. Proft T., Baker E. N. (2009). Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease. Cell. Mol. Life Sci. 66 613–635. 10.1007/s00018-008-8477-4
    1. Pumbwe L., Skilbeck C. A., Wexler H. M. (2006). The Bacteroides fragilis cell envelope: quarterback, linebacker, coach—or all three? Anaerobe 12 211–220. 10.1016/j.anaerobe.2006.09.004
    1. Riedel C. U., Foata F., Goldstein D. R., Blum S., Eikmanns B. J. (2006). Interaction of bifidobacteria with Caco-2 cells-adhesion and impact on expression profiles. Int. J. Food Microbiol. 110 62–68. 10.1016/j.ijfoodmicro.2006.01.040
    1. Ruas-Madiedo P., Gueimonde M., Margolles A., de los Reyes-Gavilán C. G., Salminen S. (2006). Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J. Food Prot. 69 2011–2015.
    1. Ruiz L., Couté Y., Sánchez B., de los Reyes-Gavilán C. G., Sanchez J.-C., Margolles A. (2009). The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology 155 957–967. 10.1099/mic.0.024273-0
    1. Savijoki K., Suokko A., Palva A., Valmu L., Kalkkinen N., Varmanen P. (2005). Effect of heat-shock and bile salts on protein synthesis of Bifidobacterium longum revealed by [35S]methionine labelling and two-dimensional gel electrophoresis. FEMS Microbiol. Lett. 248 207–215. 10.1016/j.femsle.2005.05.032
    1. Sears C. L., Geis A. L., Housseau F. (2014). Bacteroides fragilis subverts mucosal biology: from symbiont to colon carcinogenesis. J. Clin. Invest. 124 4166–4172. 10.1172/JCI72334
    1. Serafini F., Strati F., Ruas-Madiedo P., Turroni F., Foroni E., Duranti S., et al. (2013). Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010. Anaerobe 21 9–17. 10.1016/j.anaerobe.2013.03.003
    1. Sivan A., Corrales L., Hubert N., Williams J. B., Aquino-Michaels K., Earley Z. M., et al. (2015). Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350 1084–1089. 10.1126/science.aac4255
    1. Stavru F., Archambaud C., Cossart P. (2011). Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 240 160–184. 10.1111/j.1600-065X.2010.00993.x
    1. Tailford L. E., Crost E. H., Kavanaugh D., Juge N. (2015). Mucin glycan foraging in the human gut microbiome. Front. Genet. 6:81 10.3389/fgene.2015.00081
    1. Tan F. Y. Y., Tang C. M., Exley R. M. (2015). Sugar coating: bacterial protein glycosylation and host–microbe interactions. Trends Biochem. Sci. 40 342–350. 10.1016/j.tibs.2015.03.016
    1. Telford J. L., Barocchi M. A., Margarit I., Rappuoli R., Grandi G. (2006). Pili in gram-positive pathogens. Nat. Rev. Microbiol. 4 509–519. 10.1038/nrmicro1443
    1. Tuomola E., Crittenden R., Playne M., Isolauri E., Salminen S. (2001). Quality assurance criteria for probiotic bacteria. Am. J. Clin. Nutr. 73 393S–398S.
    1. Turroni F., Serafini F., Foroni E., Duranti S., O’Connell Motherway M., Taverniti V., et al. (2013). Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. Proc. Natl. Acad. Sci. U.S.A. 110 11151–11156. 10.1073/pnas.1303897110
    1. Turroni F., Serafini F., Mangifesta M., Arioli S., Mora D., van Sinderen D., et al. (2014). Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions. FEMS Microbiol. Lett. 357 23–33. 10.1111/1574-6968.12509
    1. Tytgat H. L. P., Lebeer S. (2014). The sweet tooth of bacteria: common themes in bacterial glycoconjugates. Microbiol. Mol. Biol. Rev. 78 372–417. 10.1128/MMBR.00007-14
    1. van Tassell M. L., Miller M. J. (2011). Lactobacillus adhesion to mucus. Nutrients 3 613–636. 10.3390/nu3050613
    1. Vélez M. P., De Keersmaecker S. C. J., Vanderleyden J. (2007). Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276 140–148. 10.1111/j.1574-6968.2007.00908.x
    1. Ventura M., Turroni F., Zomer A., Foroni E., Giubellini V., Bottacini F., et al. (2009). The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet. 5:e1000785 10.1371/journal.pgen.1000785
    1. Walker A. W., Martin J. C., Scott P., Parkhill J., Flint H. J., Scott K. P. (2015). 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome 3 26 10.1186/s40168-015-0087-4
    1. 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 10.3389/fmicb.2016.00097
    1. Wei X., Yan X., Chen X., Yang Z., Li H., Zou D., et al. (2014). Proteomic analysis of the interaction of Bifidobacterium longum NCC2705 with the intestine cells Caco-2 and identification of plasminogen receptors. J. Proteomics 108 89–98. 10.1016/j.jprot.2014.04.038
    1. Weidenmaier C., Peschel A. (2008). Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6 276–287. 10.1038/nrmicro1861
    1. Westermann C., Zhurina D. S., Baur A., Shang W., Yuan J., Riedel C. U. (2012). Exploring the genome sequence of Bifidobacterium bifidum S17 for potential players in host-microbe interactions. Symbiosis 58 191–200. 10.1007/s13199-012-0205-z
    1. Wexler H. M. (2007). Bacteroides: the good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20 593–621. 10.1128/CMR.00008-07
    1. Whelan K., Quigley E. M. M. (2013). Probiotics in the management of irritable bowel syndrome and inflammatory bowel disease. Curr. Opin. Gastroenterol. 29 184–189. 10.1097/MOG.0b013e32835d7bba
    1. Yatsunenko T., Rey F. E., Manary M. J., Trehan I., Dominguez-Bello M. G., Contreras M., et al. (2012). Human gut microbiome viewed across age and geography. Nature 486 222–227. 10.1038/nature11053
    1. Yuan J., Wang B., Sun Z., Bo X., Yuan X., He X., et al. (2008). Analysis of host-inducing proteome changes in bifidobacterium longum NCC2705 grown in Vivo. J. Proteome Res. 7 375–385. 10.1021/pr0704940
    1. Yuan J., Zhu L., Liu X., Li T., Zhang Y., Ying T., et al. (2006). A proteome reference map and proteomic analysis of Bifidobacterium longum NCC2705. Mol. Cell. Proteomics 5 1105–1118. 10.1074/mcp.M500410-MCP200
    1. Zhu D., Sun Y., Liu F., Li A., Yang L., Meng X.-C. (2016). Identification of surface-associated proteins of Bifidobacterium animalis ssp. lactis KLDS 2.0603 by enzymatic shaving. J. Dairy Sci. 99 5155–5172. 10.3168/jds.2015-10581
    1. Zhurina D., Dudnik A., Waidmann M. S., Grimm V., Westermann C., Breitinger K. J., et al. (2013). High-quality draft genome sequence of Bifidobacterium longum E18, isolated from a healthy adult. Genome Announc. 1 e1084-13 10.1128/genomeA.01084-13

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