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Lactobacillus Biofilms Influence Anti-Candida Activity
Language
English
Obiettivo Specifico
3IT. Calcolo scientifico
Status
Published
JCR Journal
JCR Journal
Peer review journal
Yes
Title of the book
Issue/vol(year)
/12 (2021)
Publisher
Frontiers Media S.A.
Pages (printed)
750368
Issued date
October 29, 2021
Alternative Location
Subjects
Abstract
Lactobacilli are the dominant members of the healthy human vaginal microbiota and represent the first defense line from pathogen infection, including vulvovaginal candidiasis. Biofilm is the predominant microbial growth form in nature, and the formation of biofilms inside the human body has important implications in health and disease. In particular, the formation of biofilm by members of the human resident microbiota is desirable, as it can improve microbial persistence and influence functionality. In the present study, we investigated the capability of 16 vaginal Lactobacillus strains (belonging to Lactobacillus crispatus, Lactobacillus gasseri, Lactobacillus vaginalis, and Lactobacillus plantarum species) to form biofilms, and we correlated their mode of growth to anti-Candida activity. L. plantarum strains were the best biofilm producers, and high variability was registered in the level of biofilm formation among L. crispatus and L. gasseri strains. Culture supernatants derived from Lactobacillus biofilm and planktonic growth were tested toward a panel of Candida clinical isolates (Candida albicans, Candida glabrata, Candida lusitaniae, Candida tropicalis, Candida krusei, and Candida parapsilosis) and their metabolome assessed by 1H-NMR. L. crispatus and L. plantarum strains exhibited the best fungistatic profile, and biofilms enhanced their anti-Candida activity; on the contrary, L. gasseri strains were more effective when grown in a planktonic mode. Biofilm/planktonic mode of growth also affects Lactobacillus metabolism, mainly influencing nitrogen and amino acid pathways, and anti-Candida activity is instead strictly related to carbohydrate metabolism. The present study underlined the strict interdependence between microbial mode of growth, metabolism, and functional properties. Biofilm formation by members of the healthy human microbiota represents a crucial issue in the field of microbial physiology and host-microbiota interactions, beyond supporting the development of new antimycotic strategies based on probiotics grown in adherence.
References
Abruzzo, A., Giordani, B., Parolin, C., De Gregorio, P. R., Foschi, C., Cerchiara, T., et al. (2021). Lactobacillus crispatus BC1 biosurfactant delivered by hyalurosomes: an advanced strategy to counteract candida biofilm. Antibiotics 10:33. doi: 10.3390/antibiotics10010033
Abruzzo, A., Giordani, B., Parolin, C., Vitali, B., Protti, M., Mercolini, L., et al. (2018). Novel mixed vesicles containing lactobacilli biosurfactant for vaginal delivery of an anti- Candida agent. Eur. J. Pharm. Sci. 112, 95–101. doi: 10.1016/j.ejps.2017.11.012
Aoudia, N., Rieu, A., Briandet, R., Deschamps, J., Chluba, J., Jego, G., et al. (2016). Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol. 53, 51–59. doi: 10.1016/j.fm.2015.04.009
Boskey, E. R., Cone, R. A., Whaley, K. J., and Moench, T. R. (2001). Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum. Reprod. 16, 1809–1813. doi: 10.1093/humrep/16.9.1809
Calonghi, N., Parolin, C., Sartor, G., Verardi, L., Giordani, B., Frisco, G., et al. (2017). Interaction of vaginal Lactobacillus strains with HeLa cells plasma membrane. Benef. Microbes 8, 625–633. doi: 10.3920/BM2016.0212
Ceccarani, C., Foschi, C., Parolin, C., D’Antuono, A., Gaspari, V., Consolandi, C., et al. (2019). Diversity of vaginal microbiome and metabolome during genital infections. Sci. Rep. 9:14095. doi: 10.1038/s41598-019-50410-x
EUCAST Committee (2020). Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. E. Def. 7.3. 2, 1–21.
De Gregorio, P., Silva, J., Marchesi, A., and Nader-Macías, M. (2019). Anti-Candida activity of beneficial vaginal lactobacilli in in vitro assays and in a murine experimental model. FEMS Yeast Res. 19:foz008.
Donlan, R. M., and Costerton, J. W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193. doi: 10.1128/CMR.15.2.167-193.2002
Flemming, H. C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633. doi: 10.1038/nrmicro2415
Jang, S. J., Lee, K., Kwon, B., You, H. J., and Ko, G. P. (2019). Vaginal lactobacilli inhibit growth and hyphae formation of Candida albicans. Sci. Rep. 9:8121. doi: 10.1038/s41598-019-44579-4
Kleerebezem, M., Boekhorst, J., Van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., et al. (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. U. S. A. 100, 1990–1995. doi: 10.1073/pnas.0337704100
Kubota, H., Senda, S., Nomura, N., Tokuda, H., and Uchiyama, H. (2008). Biofilm Formation by Lactic Acid Bacteria and Resistance to Environmental Stress. J. Biosci. Bioeng. 106, 381–386. doi: 10.1263/jbb.106.381
Laghi, L., Picone, G., Cruciani, F., Brigidi, P., Calanni, F., Donders, G., et al. (2014). Rifaximin modulates the vaginal microbiome and metabolome in women affected by bacterial vaginosis. Antimicrob. Agents Chemother. 58, 3411–3420. doi: 10.1128/AAC.02469-14
Leccese Terraf, M. C., Mendoza, L. M., Juárez Tomás, M. S., Silva, C., and Nader-Macías, M. E. F. (2014). Phenotypic surface properties (aggregation, adhesion and biofilm formation) and presence of related genes in beneficial vaginal lactobacilli. J. Appl. Microbiol. 117, 1761–1772. doi: 10.1111/jam.12642
Li, Z., Behrens, A. M., Ginat, N., Tzeng, S. Y., Lu, X., Sivan, S., et al. (2018). Biofilm-inspired encapsulation of probiotics for the treatment of complex infections. Adv. Mater. 30:e1803925. doi: 10.1002/adma.201803925
Liu, L., Guo, S., Chen, X., Yang, S., Deng, X., Tu, M., et al. (2021). Metabolic profiles of Lactobacillus paraplantarum in biofilm and planktonic states and investigation of its intestinal modulation and immunoregulation in dogs. Food Funct. 12, 5317–5332. doi: 10.1039/d1fo00905b
Liu, L., Wu, R., Zhang, J., and Li, P. (2018). Overexpression of luxSPromotes stress resistance and biofilm Formation of lactobacillus paraplantarumL-ZS9 by regulating the expression of multiple genes. Front. Microbiol. 9:2628. doi: 10.3389/fmicb.2018.02628
Namarta, K., Jatinder, S., and Manpreet, K. (2020). Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: a critical review. Ann. Clin. Microbiol. Antimicrob. 19:5. doi: 10.1186/s12941-020-0347-4
Nardini, P., Ñahui Palomino, R. A., Parolin, C., Laghi, L., Foschi, C., Cevenini, R., et al. (2016). Lactobacillus crispatus inhibits the infectivity of Chlamydia trachomatis elementary bodies, in vitro study. Sci. Rep. 6:29024. doi: 10.1038/srep29024
O’Hanlon, D. E., Moench, T. R., and Cone, R. A. (2013). Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS One 8:e80074. doi: 10.1371/journal.pone.0080074
Oliver, J. C., Laghi, L., Parolin, C., Foschi, C., Marangoni, A., Liberatore, A., et al. (2020). Metabolic profiling of Candida clinical isolates of different species and infection sources. Sci. Rep. 10:16716. doi: 10.1038/s41598-020-73889-1
Parolin, C., Abruzzo, A., Giordani, B., Oliver, J. C., Marangoni, A., Luppi, B., et al. (2021). Anti-candida activity of hyaluronic acid combined with lactobacillus crispatus lyophilised supernatant: a new antifungal strategy. Antibiotics 10:628. doi: 10.3390/antibiotics10060628
Parolin, C., Marangoni, A., Laghi, L., Foschi, C., Palomino, R. A. Ñ, Calonghi, N., et al. (2015). Isolation of vaginal lactobacilli and characterization of anti-candida activity. PLoS One 10:e0131220. doi: 10.1371/journal.pone.0131220
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., et al. (2011). Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 108, 4680–4687. doi: 10.1073/pnas.1002611107
Rieu, A., Aoudia, N., Jego, G., Chluba, J., Yousfi, N., Briandet, R., et al. (2014). The biofilm mode of life boosts the anti-inflammatory properties of Lactobacillus. Cell. Microbiol. 16, 1836–1853. doi: 10.1111/cmi.12331
Rodrigues, C. F., Silva, S., and Henriques, M. (2014). Candida glabrata: a review of its features and resistance. Eur. J. Clin. Microbiol. Infect. Dis. 33, 673–688. doi: 10.1007/s10096-013-2009-3
Rönnqvist, D., Forsgren-Brusk, B., and EGrahn-Håkansson, E. (2006). Lactobacilli in the female genital tract in relation to other genital microbes and vaginal pH. Acta Obstet. Gynecol. Scand. 85, 726–735. doi: 10.1080/00016340600578357
Salas-Jara, M., Ilabaca, A., Vega, M., and García, A. (2016). Biofilm Forming Lactobacillus: new Challenges for the Development of Probiotics. Microorganisms 4:35. doi: 10.3390/microorganisms4030035
Stivala, A., Carota, G., Fuochi, V., and Furneri, P. M. (2021). Lactobacillus rhamnosus AD3 as a promising alternative for probiotic products. Biomolecules 11:94. doi: 10.3390/biom11010094
Sturme, M. H. J., Nakayama, J., Molenaar, D., Murakami, Y., Kunugi, R., Fujii, T., et al. (2005). An agr-like two-component regulatory system in Lactobacillus plantarum is involved in production of a novel cyclic peptide and regulation of adherence. J. Bacteriol. 187, 5224–5235. doi: 10.1128/JB.187.15.5224-5235.2005
Tortelli, B., Lewis, W., Allsworth, J., Member-Meneh, N., Foster, L., Reno, H., et al. (2020). Associations between the vaginal microbiome and Candida colonization in women of reproductive age. Physiol. Behav. 176, 139–148. doi: 10.1016/j.ajog.2019.10.008.Associations
van den Nieuwboer, M., van Hemert, S., Claassen, E., and de Vos, W. M. (2016). Lactobacillus plantarum WCFS1 and its host interaction: a dozen years after the genome. Microb. Biotechnol. 9, 452–465. doi: 10.1111/1751-7915.12368
Van der Maaten, L., and Hinton, G. (2008). Multiobjective evolutionary algorithms to identify highly autocorrelated areas: the case of spatial distribution in financially compromised farms. Ann. Oper. Res. 219, 187–202. doi: 10.1007/s10479-011-0841-3
van der Veer, C., Hertzberger, R. Y., Bruisten, S. M., Tytgat, H. L. P., Swanenburg, J., Angelino-Bart, A., et al. (2018). Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota. bioRxiv [Preprint]. doi: 10.1101/441972
Ventolini, G. (2015). Vaginal lactobacillus: biofilm formation in vivo – clinical implications. Int. J. Womens. Health 7, 243–247. doi: 10.2147/IJWH.S77956
Wang, S., Wang, Q., Yang, E., Yan, L., Li, T., and Zhuang, H. (2017). Antimicrobial compounds produced by vaginal Lactobacillus crispatus are able to strongly inhibit Candida albicans growth, hyphal formation and regulate virulence-related gene expressions. Front. Microbiol. 8:564. doi: 10.3389/fmicb.2017.00564
Abruzzo, A., Giordani, B., Parolin, C., Vitali, B., Protti, M., Mercolini, L., et al. (2018). Novel mixed vesicles containing lactobacilli biosurfactant for vaginal delivery of an anti- Candida agent. Eur. J. Pharm. Sci. 112, 95–101. doi: 10.1016/j.ejps.2017.11.012
Aoudia, N., Rieu, A., Briandet, R., Deschamps, J., Chluba, J., Jego, G., et al. (2016). Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol. 53, 51–59. doi: 10.1016/j.fm.2015.04.009
Boskey, E. R., Cone, R. A., Whaley, K. J., and Moench, T. R. (2001). Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum. Reprod. 16, 1809–1813. doi: 10.1093/humrep/16.9.1809
Calonghi, N., Parolin, C., Sartor, G., Verardi, L., Giordani, B., Frisco, G., et al. (2017). Interaction of vaginal Lactobacillus strains with HeLa cells plasma membrane. Benef. Microbes 8, 625–633. doi: 10.3920/BM2016.0212
Ceccarani, C., Foschi, C., Parolin, C., D’Antuono, A., Gaspari, V., Consolandi, C., et al. (2019). Diversity of vaginal microbiome and metabolome during genital infections. Sci. Rep. 9:14095. doi: 10.1038/s41598-019-50410-x
EUCAST Committee (2020). Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. E. Def. 7.3. 2, 1–21.
De Gregorio, P., Silva, J., Marchesi, A., and Nader-Macías, M. (2019). Anti-Candida activity of beneficial vaginal lactobacilli in in vitro assays and in a murine experimental model. FEMS Yeast Res. 19:foz008.
Donlan, R. M., and Costerton, J. W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193. doi: 10.1128/CMR.15.2.167-193.2002
Flemming, H. C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633. doi: 10.1038/nrmicro2415
Jang, S. J., Lee, K., Kwon, B., You, H. J., and Ko, G. P. (2019). Vaginal lactobacilli inhibit growth and hyphae formation of Candida albicans. Sci. Rep. 9:8121. doi: 10.1038/s41598-019-44579-4
Kleerebezem, M., Boekhorst, J., Van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., et al. (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. U. S. A. 100, 1990–1995. doi: 10.1073/pnas.0337704100
Kubota, H., Senda, S., Nomura, N., Tokuda, H., and Uchiyama, H. (2008). Biofilm Formation by Lactic Acid Bacteria and Resistance to Environmental Stress. J. Biosci. Bioeng. 106, 381–386. doi: 10.1263/jbb.106.381
Laghi, L., Picone, G., Cruciani, F., Brigidi, P., Calanni, F., Donders, G., et al. (2014). Rifaximin modulates the vaginal microbiome and metabolome in women affected by bacterial vaginosis. Antimicrob. Agents Chemother. 58, 3411–3420. doi: 10.1128/AAC.02469-14
Leccese Terraf, M. C., Mendoza, L. M., Juárez Tomás, M. S., Silva, C., and Nader-Macías, M. E. F. (2014). Phenotypic surface properties (aggregation, adhesion and biofilm formation) and presence of related genes in beneficial vaginal lactobacilli. J. Appl. Microbiol. 117, 1761–1772. doi: 10.1111/jam.12642
Li, Z., Behrens, A. M., Ginat, N., Tzeng, S. Y., Lu, X., Sivan, S., et al. (2018). Biofilm-inspired encapsulation of probiotics for the treatment of complex infections. Adv. Mater. 30:e1803925. doi: 10.1002/adma.201803925
Liu, L., Guo, S., Chen, X., Yang, S., Deng, X., Tu, M., et al. (2021). Metabolic profiles of Lactobacillus paraplantarum in biofilm and planktonic states and investigation of its intestinal modulation and immunoregulation in dogs. Food Funct. 12, 5317–5332. doi: 10.1039/d1fo00905b
Liu, L., Wu, R., Zhang, J., and Li, P. (2018). Overexpression of luxSPromotes stress resistance and biofilm Formation of lactobacillus paraplantarumL-ZS9 by regulating the expression of multiple genes. Front. Microbiol. 9:2628. doi: 10.3389/fmicb.2018.02628
Namarta, K., Jatinder, S., and Manpreet, K. (2020). Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: a critical review. Ann. Clin. Microbiol. Antimicrob. 19:5. doi: 10.1186/s12941-020-0347-4
Nardini, P., Ñahui Palomino, R. A., Parolin, C., Laghi, L., Foschi, C., Cevenini, R., et al. (2016). Lactobacillus crispatus inhibits the infectivity of Chlamydia trachomatis elementary bodies, in vitro study. Sci. Rep. 6:29024. doi: 10.1038/srep29024
O’Hanlon, D. E., Moench, T. R., and Cone, R. A. (2013). Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS One 8:e80074. doi: 10.1371/journal.pone.0080074
Oliver, J. C., Laghi, L., Parolin, C., Foschi, C., Marangoni, A., Liberatore, A., et al. (2020). Metabolic profiling of Candida clinical isolates of different species and infection sources. Sci. Rep. 10:16716. doi: 10.1038/s41598-020-73889-1
Parolin, C., Abruzzo, A., Giordani, B., Oliver, J. C., Marangoni, A., Luppi, B., et al. (2021). Anti-candida activity of hyaluronic acid combined with lactobacillus crispatus lyophilised supernatant: a new antifungal strategy. Antibiotics 10:628. doi: 10.3390/antibiotics10060628
Parolin, C., Marangoni, A., Laghi, L., Foschi, C., Palomino, R. A. Ñ, Calonghi, N., et al. (2015). Isolation of vaginal lactobacilli and characterization of anti-candida activity. PLoS One 10:e0131220. doi: 10.1371/journal.pone.0131220
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., et al. (2011). Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 108, 4680–4687. doi: 10.1073/pnas.1002611107
Rieu, A., Aoudia, N., Jego, G., Chluba, J., Yousfi, N., Briandet, R., et al. (2014). The biofilm mode of life boosts the anti-inflammatory properties of Lactobacillus. Cell. Microbiol. 16, 1836–1853. doi: 10.1111/cmi.12331
Rodrigues, C. F., Silva, S., and Henriques, M. (2014). Candida glabrata: a review of its features and resistance. Eur. J. Clin. Microbiol. Infect. Dis. 33, 673–688. doi: 10.1007/s10096-013-2009-3
Rönnqvist, D., Forsgren-Brusk, B., and EGrahn-Håkansson, E. (2006). Lactobacilli in the female genital tract in relation to other genital microbes and vaginal pH. Acta Obstet. Gynecol. Scand. 85, 726–735. doi: 10.1080/00016340600578357
Salas-Jara, M., Ilabaca, A., Vega, M., and García, A. (2016). Biofilm Forming Lactobacillus: new Challenges for the Development of Probiotics. Microorganisms 4:35. doi: 10.3390/microorganisms4030035
Stivala, A., Carota, G., Fuochi, V., and Furneri, P. M. (2021). Lactobacillus rhamnosus AD3 as a promising alternative for probiotic products. Biomolecules 11:94. doi: 10.3390/biom11010094
Sturme, M. H. J., Nakayama, J., Molenaar, D., Murakami, Y., Kunugi, R., Fujii, T., et al. (2005). An agr-like two-component regulatory system in Lactobacillus plantarum is involved in production of a novel cyclic peptide and regulation of adherence. J. Bacteriol. 187, 5224–5235. doi: 10.1128/JB.187.15.5224-5235.2005
Tortelli, B., Lewis, W., Allsworth, J., Member-Meneh, N., Foster, L., Reno, H., et al. (2020). Associations between the vaginal microbiome and Candida colonization in women of reproductive age. Physiol. Behav. 176, 139–148. doi: 10.1016/j.ajog.2019.10.008.Associations
van den Nieuwboer, M., van Hemert, S., Claassen, E., and de Vos, W. M. (2016). Lactobacillus plantarum WCFS1 and its host interaction: a dozen years after the genome. Microb. Biotechnol. 9, 452–465. doi: 10.1111/1751-7915.12368
Van der Maaten, L., and Hinton, G. (2008). Multiobjective evolutionary algorithms to identify highly autocorrelated areas: the case of spatial distribution in financially compromised farms. Ann. Oper. Res. 219, 187–202. doi: 10.1007/s10479-011-0841-3
van der Veer, C., Hertzberger, R. Y., Bruisten, S. M., Tytgat, H. L. P., Swanenburg, J., Angelino-Bart, A., et al. (2018). Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: implications for in vivo dominance of the vaginal microbiota. bioRxiv [Preprint]. doi: 10.1101/441972
Ventolini, G. (2015). Vaginal lactobacillus: biofilm formation in vivo – clinical implications. Int. J. Womens. Health 7, 243–247. doi: 10.2147/IJWH.S77956
Wang, S., Wang, Q., Yang, E., Yan, L., Li, T., and Zhuang, H. (2017). Antimicrobial compounds produced by vaginal Lactobacillus crispatus are able to strongly inhibit Candida albicans growth, hyphal formation and regulate virulence-related gene expressions. Front. Microbiol. 8:564. doi: 10.3389/fmicb.2017.00564
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