Streptococcus dentisani inhibits the growth of Candida albicans and Candida glabrata: in vitro assay.

Candida Streptococcus dentisani Biofilm Oral cavity Oral dysbiosis

Journal

International microbiology : the official journal of the Spanish Society for Microbiology
ISSN: 1618-1905
Titre abrégé: Int Microbiol
Pays: Switzerland
ID NLM: 9816585

Informations de publication

Date de publication:
07 Jun 2024
Historique:
received: 20 01 2024
accepted: 03 05 2024
revised: 01 05 2024
medline: 7 6 2024
pubmed: 7 6 2024
entrez: 6 6 2024
Statut: aheadofprint

Résumé

Probiotic bacteria inhibit aggregation, biofilm formation, and dimorphism of Candida spp. However, the effects of a new probiotic, Streptococcus dentisani, on the growth of Candida albicans and Candida glabrata biofilms are unknown. To determine the effect of S. dentisani on the different phases of C. albicans and C. glabrata biofilm development. Growth quantification and ultrastructural analyses were performed on biofilms of C. albicans ATCC 90028, C. glabrata ATCC 2001, and clinical isolates of C. albicans from oral candidiasis (CA-C1), caries (CA-CR1), and periodontal pocket (CA-P1) treated with cell suspensions of S. dentisani CECT 7746. Cell viability was determined by quantifying colony-forming units (CFU/mL). The ultrastructural analyses were done with atomic force microscopy. S. dentisani induced a significant reduction (p < 0.05) of CFU/mL of immature and mature biofilm in all strains of C. albicans and C. glabrata. Microscopic analysis revealed that S. dentisani reduced C. albicans density in mixed biofilm. The fungus-bacteria interaction affected cell membrane integrity in yeast. For the first time, our data elucidate the antifungal effect of S. dentisani on the development of C. albicans and C. glabrata biofilms, supporting its usefulness as a niche-specific probiotic to prevent and treat oral dysbiosis.

Sections du résumé

BACKGROUND BACKGROUND
Probiotic bacteria inhibit aggregation, biofilm formation, and dimorphism of Candida spp. However, the effects of a new probiotic, Streptococcus dentisani, on the growth of Candida albicans and Candida glabrata biofilms are unknown.
OBJECTIVE OBJECTIVE
To determine the effect of S. dentisani on the different phases of C. albicans and C. glabrata biofilm development.
METHODS METHODS
Growth quantification and ultrastructural analyses were performed on biofilms of C. albicans ATCC 90028, C. glabrata ATCC 2001, and clinical isolates of C. albicans from oral candidiasis (CA-C1), caries (CA-CR1), and periodontal pocket (CA-P1) treated with cell suspensions of S. dentisani CECT 7746. Cell viability was determined by quantifying colony-forming units (CFU/mL). The ultrastructural analyses were done with atomic force microscopy.
RESULTS RESULTS
S. dentisani induced a significant reduction (p < 0.05) of CFU/mL of immature and mature biofilm in all strains of C. albicans and C. glabrata. Microscopic analysis revealed that S. dentisani reduced C. albicans density in mixed biofilm. The fungus-bacteria interaction affected cell membrane integrity in yeast.
CONCLUSION CONCLUSIONS
For the first time, our data elucidate the antifungal effect of S. dentisani on the development of C. albicans and C. glabrata biofilms, supporting its usefulness as a niche-specific probiotic to prevent and treat oral dysbiosis.

Identifiants

pubmed: 38844735
doi: 10.1007/s10123-024-00525-7
pii: 10.1007/s10123-024-00525-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Switzerland AG.

Références

Azad A, Ranjbaran A, Zareshahrabadi Z et al (2021) Protective effects of the probiotic bacterium Streptococcus thermophilus on Candida albicans morphogenesis and a murine model of oral candidiasis. Iran J Med Sci 46(3):207–217. https://doi.org/10.30476/ijms.2020.82080.0
doi: 10.30476/ijms.2020.82080.0 pubmed: 34083853 pmcid: 8163705
Camelo-Castillo A, Benítez-Páez A, Belda-Ferre P et al (2014) A. Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 64:60–65. https://doi.org/10.1099/ijs.0.054098-0
doi: 10.1099/ijs.0.054098-0 pubmed: 24006481
Cavalheiro M, Teixeira MC (2018) Candida biofilms: threats, challenges, and promising strategies. Front Med (lausanne) 13(5):28
doi: 10.3389/fmed.2018.00028
Conrads G, Westenberger J, Lürkens M et al (2019) Isolation and bacteriocin-related typing of Streptococcus dentisani. Front Cell Infect Microbiol 16(9):110. https://doi.org/10.3389/fcimb.2019.00110
doi: 10.3389/fcimb.2019.00110
d’Enfert C, Kaune AK, Alaban LR et al (2021) The impact of the Fungus-Host-Microbiota interplay upon Candida albicans infections: current knowledge and new perspectives. FEMS Microbiol Rev 45:060. https://doi.org/10.1093/femsre/fuaa060
doi: 10.1093/femsre/fuaa060
Diaz PI, Dongari-Bagtzoglou A (2021) Critically appraising the significance of the oral mycobiome. J Dent Res 100(2):133–140. https://doi.org/10.1177/0022034520956975
doi: 10.1177/0022034520956975 pubmed: 32924741
Diaz PI, Xie Z, Sobue T et al (2012) Synergistic interaction between Candida albicans and commensal oral streptococci in a novel in vitro mucosal model. Infect Immun 80(2):620–632. https://doi.org/10.1128/IAI.05896-11
doi: 10.1128/IAI.05896-11 pubmed: 22104105 pmcid: 3264323
Esteban-Fernández A, Ferrer MD, Zorraquín-Peña I et al (2019) In vitro beneficial effects of Streptococcus dentisani as potential oral probiotic for periodontal diseases. J Periodontol 90(11):1346–1355. https://doi.org/10.1002/JPER.18-0751
doi: 10.1002/JPER.18-0751 pubmed: 31111495
Frías-De-León MG, Hernández-Castro R, Conde-Cuevas E et al (2021) Candida glabrata antifungal resistance and virulence factors, a perfect pathogenic combination. Pharmaceutics 13(10):1529. https://doi.org/10.3390/pharmaceutics13101529
doi: 10.3390/pharmaceutics13101529 pubmed: 34683822 pmcid: 8538829
Koopman JE, Röling WF, Buijs MJ et al (2015) Stability and resilience of oral microcosms toward acidification and Candida outgrowth by arginine supplementation. Microb Ecol 69(2):422–433. https://doi.org/10.1007/s00248-014-0535-x
doi: 10.1007/s00248-014-0535-x pubmed: 25433583
Krzyściak W, Kościelniak D, Papież M et al (2017) Effect of a Lactobacillus salivarius probiotic on a double-species Streptococcus mutans and Candida albicans caries biofilm. Nutrients 9(11):1242. https://doi.org/10.3390/nu9111242
doi: 10.3390/nu9111242 pubmed: 29135948 pmcid: 5707714
Llena C, Almarche A, Mira A et al (2019) Antimicrobial efficacy of the supernatant of Streptococcus dentisani against microorganisms implicated in root canal infections. J Oral Sci 61(1):184–194. https://doi.org/10.2334/josnusd.18-0239
doi: 10.2334/josnusd.18-0239 pubmed: 30918216
López-López A, Camelo-Castillo A, Ferrer MD et al (2017) Health-associated niche inhabitants as oral probiotics: the case of Streptococcus dentisani. Front Microbiol 8:379. https://doi.org/10.3389/fmicb.2017.00379
doi: 10.3389/fmicb.2017.00379 pubmed: 28344574 pmcid: 5344910
Martorano-Fernandes L, Rodrigues NC, de Souza Borges MH et al (2020) Interkingdom interaction between C. albicans and S. salivarius on titanium surfaces. BMC Oral Health 20(1):349. https://doi.org/10.1186/s12903-020-01334-w
doi: 10.1186/s12903-020-01334-w pubmed: 33261593 pmcid: 7706213
Matsubara VH (2016) Probiotic lactobacilli inhibit early stages of Candida albicans biopelícula development by reducing their growth, cell adhesion, and filamentation. Appl Microbiol Biotechnol 100(14):6415–6426. https://doi.org/10.1007/s00253-016-7527-3
doi: 10.1007/s00253-016-7527-3 pubmed: 27087525
Mead R (2012) Cambridge University Press -Statistical principles for the design of experiments. https://assets.cambridge.org/97805218/62141/frontmatter/9780521862141_frontmatter.pdf . Acceso 08 October 2021
Mokhtar M, Rismayuddin NAR, Mat Yassim AS et al (2021) Streptococcus salivarius K12 inhibits Candida albicans aggregation, biofilm formation and dimorphism. Biofouling 37(7):767–776. https://doi.org/10.1080/08927014.2021.1967334
doi: 10.1080/08927014.2021.1967334 pubmed: 34425729
Nascimento MM (2018) Potential uses of arginine in dentistry. Adv Dent Res 29(1):98–103. https://doi.org/10.3389/fmed.2018.00028
doi: 10.3389/fmed.2018.00028 pubmed: 29355411 pmcid: 5784480
Paltanea M, Tabirca S, Scheiber E et al (2010) Logarithmic growth in biological processes. 2010 12th International conference on computer modelling and simulation. Cambridge, UK, pp 116–121. https://doi.org/10.1109/UKSIM.2010.29
Pandey KR, Naik SR, Vakil BV (2015) Probiotics, prebiotics and synbiotics - a review. J Food Sci Technol 52(12):7577–7587. https://doi.org/10.1007/s13197-015-1921-1
doi: 10.1007/s13197-015-1921-1 pubmed: 26604335 pmcid: 4648921
Rossoni RD, de Barros PP, de Alvarenga JA et al (2018) Antifungal activity of clinical Lactobacillus strains against Candida albicans biofilms: identification of potential probiotic candidates to prevent oral candidiasis. Biofouling 34(2):212–225. https://doi.org/10.1080/08927014.2018.1425402
doi: 10.1080/08927014.2018.1425402 pubmed: 29380647
Serpa Sampaio Moreno L, Nobre Junior HV, Ramos da Silva A et al (2021) Arginine-phenylalanine and arginine-tryptophan-based surfactants as new biocompatible antifungal agents and their synergistic effect with Amphotericin B against fluconazole-resistant Candida strains. Colloids Surf B Biointerfaces 207:112017. https://doi.org/10.1016/j.colsurfb.2021.112017
doi: 10.1016/j.colsurfb.2021.112017 pubmed: 34391169
Srivastava N, Ellepola K, Venkiteswaran N et al (2020) Lactobacillus plantarum 108 inhibits Streptococcus mutans and Candida albicans mixed-species biofilm formation. Antibiotics (basel, Switzerland) 9(8):478. https://doi.org/10.3390/antibiotics9080478
doi: 10.3390/antibiotics9080478 pubmed: 32759754
Taniguchi M, Ochiai A, Takahashi K et al (2016) Effect of alanine, leucine, and arginine substitution on antimicrobial activity against candida albicans and action mechanism of a cationic octadecapeptide derived from α-amylase of rice. Biopolymers 106(2):219–229. https://doi.org/10.1002/bip.22817
doi: 10.1002/bip.22817 pubmed: 26850838
Thomas P, Sekhar AC, Upreti R et al (2015) (2015) Optimization of single plate-serial dilution spotting (SP-SDS) with sample anchoring as an assured method for bacterial and yeast cfu enumeration and single colony isolation from diverse samples. Biotechnol Rep 20:45–55. https://doi.org/10.1016/j.btre.2015.08.003
doi: 10.1016/j.btre.2015.08.003
Xu H, Jenkinson HF, Dongari-Bagtzoglou A (2014) Innocent until proven guilty: mechanisms and roles of Streptococcus-Candida interactions in oral health and disease. Mol Oral Microbiol 29(3):99–116. https://doi.org/10.1111/omi.12049
doi: 10.1111/omi.12049 pubmed: 24877244 pmcid: 4238848
Zaura E, Twetman S (2019) Critical appraisal of oral pre- and probiotics for caries prevention and care. Caries Res 53:514–526. https://doi.org/10.1159/000499037
doi: 10.1159/000499037 pubmed: 30947169

Auteurs

Juan Gerardo Sánchez Medina (JGS)

Department of Microbiology, Faculty of Dentistry, Autonomous University of San Luis Potosi, Manuel Nava No. 2, Col Universitaria, 78290, San Luis Potosí, S.L.P., Mexico.

José Luis Cuéllar Camacho (JLC)

Faculty of Science, Autonomous University of San Luis Potosi, San Luis Potosí, S.L.P., Mexico.

Jaime Ruiz Garcia (J)

Laboratory of Biological Physics, Physics Institute, Autonomous University of San Luis Potosí, San Luis Potosí, México.

Alex Mira (A)

Department of Health and Genomics, Oral Microbiome Lab, FISABIO Foundation, Valencia, Spain.

Rita Elizabeth Martínez Martínez (RE)

Periodontics Postgraduate Program, Faculty of Dentistry, Autonomous University of San Luis Potosi, San Luis Potosí, S.L.P., Mexico.

Mauricio Comas-García (M)

Department of Sciences, Research Center for Health Sciences and Biomedicine (CICSaB), Autonomous University of San Luis Potosi, San Luis Potosí, S.L.P., Mexico.

Arturo Garrocho Rangel (AG)

Periodontics Postgraduate Program, Faculty of Dentistry, Autonomous University of San Luis Potosi, San Luis Potosí, S.L.P., Mexico.

Amaury Pozos-Guillén (A)

Basic Sciences Laboratory, Faculty of Dentistry, Autonomous University of San Luis Potosí, San Luis Potosí, S.L.P., Mexico.

Saray Aranda Romo (SA)

Department of Microbiology, Faculty of Dentistry, Autonomous University of San Luis Potosi, Manuel Nava No. 2, Col Universitaria, 78290, San Luis Potosí, S.L.P., Mexico. sarayaranda@fest.uaslp.mx.
Periodontics Postgraduate Program, Faculty of Dentistry, Autonomous University of San Luis Potosi, San Luis Potosí, S.L.P., Mexico. sarayaranda@fest.uaslp.mx.
Diagnostic Clinic Dentistry School, Autonomous University of San Luis Potosí, San Luis Potosí, S.L.P., Mexico. sarayaranda@fest.uaslp.mx.

Classifications MeSH