Cervicovaginal Bacillus velezensis Isolate: A Potential Probiotic and an Antagonist Against Candida and Staphylococcus.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
29 Aug 2023
29 Aug 2023
Historique:
received:
10
04
2023
accepted:
10
08
2023
medline:
31
8
2023
pubmed:
29
8
2023
entrez:
29
8
2023
Statut:
epublish
Résumé
The cervicovaginal microbiota is an essential aspect of women's reproductive and overall health. In this study, we aimed to evaluate the probiotic properties of a cervicovaginal isolate, obtained from a gynecologically healthy woman and assess its antagonistic effect against various microorganisms isolated from the vagina. Cytological examination was performed using Papanicolaou staining, and the isolated microorganism was identified via 16S Ribosomal RNA Gene Sequence Analysis. Probiotic characteristics were evaluated by determining the tolerance of the isolate to low pH, different NaCl concentrations, and bile salts. Bacterial adherence to stainless steel sheets, antibiotic susceptibility, and antimicrobial activity tests were also conducted and analyzed. Antimicrobial tests and antagonistic activities were assessed through disc diffusion assays. The cervicovaginal isolate was identified as B. velezensis ON116948 and was found to be tolerant to low pH, high NaCl and 0.3% bile salts. Additionally, it exhibited adherence. With the exception of amoxicillin/clavulanic acid (AMC) (30 μg) and oxacillin (OX) (1 μg), this isolate was susceptible to all the antibiotics tested. Candida species did not grow on B. velezensis spread media, while B. velezensis was able to grow on C. albicans, C. glabrata, C. tropicalis, S. condimenti and S. epidermidis spread media with growth zones of 13.7 ± 0.6, 13.3 ± 0.6, 14.2 ± 4.4, 10.5 ± 0.5 and 16.0 ± 1.0 (around discs), respectively. Our findings suggest that the cervicovaginal B. velezensis ON116948 isolate exhibits probiotic properties and antagonistic activity. These results provide important insights into the potential use of this isolate as a probiotic for the prevention of vaginal infections.
Identifiants
pubmed: 37642756
doi: 10.1007/s00284-023-03447-1
pii: 10.1007/s00284-023-03447-1
doi:
Substances chimiques
Sodium Chloride
451W47IQ8X
Bile Acids and Salts
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
332Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Anahtar MN, Gootenberg DB, Mitchell CM, Kwon DS (2018) Cervicovaginal microbiota and reproductive health: the virtue of simplicity. Cell Host Microbe 23(2):159–168. https://doi.org/10.1016/j.chom.2018.01.013
doi: 10.1016/j.chom.2018.01.013
pubmed: 29447695
Gaspar C, Donders GG, Palmeira-de-Oliveira R, Queiroz JA, Tomaz C, Martinez-de-Oliveira J, Palmeira-de-Oliveira A (2018) Bacteriocin production of the probiotic Lactobacillus acidophilus KS400. AMB Expr. https://doi.org/10.1186/s13568-018-0679-z
doi: 10.1186/s13568-018-0679-z
Barrientos-Durán A, Fuentes-López A, de Salazar A, Plaza-Díaz J, García F (2020) Reviewing the composition of vaginal microbiota: inclusion of nutrition and probiotic factors in the maintenance of eubiosis. Nutrients 12(2):1–30. https://doi.org/10.3390/nu12020419
doi: 10.3390/nu12020419
Chen X, Huang H, Zhang S, Zhang Y, Jiang J, Qiu Y, Liu J, Wang A (2021) Bacillus velezensis wz-37, a new broad-spectrum biocontrol strain, promotes the growth of tomato seedlings. Agriculture 11(7):1–14. https://doi.org/10.3390/agriculture11070581
doi: 10.3390/agriculture11070581
Kumherová M, Veselá K, Kosová M, Mašata J, Horáčková Š, Šmidrkal J (2021) Novel potential probiotic Lactobacilli for prevention and treatment of vulvovaginal infections. Probiotics Antimicrob Prot 13(1):163–172. https://doi.org/10.1007/s12602-020-09675-2
doi: 10.1007/s12602-020-09675-2
Donmez HG, Cagan M, Fadiloglu E, Unal C, Onder SC, Beksac MS (2020) Is bacterial vaginosis associated with autoimmune antibody positivity? Cytopathology 4:298–302. https://doi.org/10.1111/cyt.12846
doi: 10.1111/cyt.12846
Donmez HG, Sahal G, Akgor U, Cagan M, Ozgul N, Beksac MS (2020) The relationship between the presence of HPV infection and biofilm formation in cervicovaginal smears. Infection 48(5):735–740. https://doi.org/10.1007/s15010-020-01478-5
doi: 10.1007/s15010-020-01478-5
pubmed: 32623704
Miller EA, Beasley DAE, Dunn RR, Archie EA (2016) Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique? Front Microbiol 7:1–13. https://doi.org/10.3389/fmicb.2016.01936
doi: 10.3389/fmicb.2016.01936
Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA 108(1):4680–4687. https://doi.org/10.1073/pnas.1002611107
doi: 10.1073/pnas.1002611107
pubmed: 20534435
Jang SJ, Lee K, Kwon B, You HJ, Ko GP (2019) Vaginal lactobacilli inhibit growth and hyphae formation of Candida albicans. Sci Rep 9(1):1–9. https://doi.org/10.1038/s41598-019-44579-4
doi: 10.1038/s41598-019-44579-4
Rabbee MF, Sarafat Ali M, Choi J, Hwang BS, Jeong SC, Baek K (2019) Bacillus velezensis: a valuable member of bioactive molecules within plant microbiomes. Molecules 24(6):1–13. https://doi.org/10.3390/molecules24061046
doi: 10.3390/molecules24061046
Khalid F, Khalid A, Fu Y, Hu Q, Zheng Y, Khan S, Wang Z (2021) Potential of Bacillus velezensis as a probiotic in animal feed: a review. J Microbiol 59(7):627–633. https://doi.org/10.1007/s12275-021-1161-1
doi: 10.1007/s12275-021-1161-1
pubmed: 34212287
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
doi: 10.1093/oxfordjournals.molbev.a040023
pubmed: 8336541
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
doi: 10.1093/molbev/msy096
pubmed: 29722887
pmcid: 5967553
Mulaw G, Sisay Tessema T, Muleta D, Tesfaye A (2019) In vitro evaluation of probiotic properties of lactic acid bacteria isolated from some traditionally fermented Ethiopian food products. Int J Microbiol 2019:7179514. https://doi.org/10.1155/2019/7179514
doi: 10.1155/2019/7179514
pubmed: 31534458
pmcid: 6732631
Nath S, Sikidar J, Roy M, Deb B (2020) In vitro screening of probiotic properties of Lactobacillus plantarum isolated from fermented milk product. Food Qual Saf 4(4):213–223. https://doi.org/10.1093/fqsafe/fyaa026
doi: 10.1093/fqsafe/fyaa026
Sanhueza E, Paredes-Osses E, González CL, García A (2015) Effect of PH in the survival of Lactobacillus salivarius strain UCO_979C wild type and the Ph acid acclimated variant. Electron J Biotechnol 18(5):343–346. https://doi.org/10.1016/j.ejbt.2015.06.005
doi: 10.1016/j.ejbt.2015.06.005
Thakkar P, Modi HA, Prajapati JB (2015) Isolation, characterization and safety assessment of lactic acid bacterial ısolates from fermented food products. Int J Curr Microbiol Appl Sci 4(4):713–725
Kang M, Su X, Yun L, Shen Y, Feng J, Yang G, Meng X, Zhang J, Chang X (2022) Evaluation of probiotic characteristics and whole genome analysis of Bacillus velezensis R-71003 isolated from the intestine of common carp (Cyprinus carpio L.) for its use as a probiotic in aquaculture. Aquacult Rep. https://doi.org/10.1016/j.aqrep.2022.101254
doi: 10.1016/j.aqrep.2022.101254
Sahal G, Bilkay IS (2015) Multidrug resistance by biofilm-forming clinical strains of Proteus mirabilis. Asian Biomed 9(4):535–554. https://doi.org/10.5372/1905-7415.0904.424
doi: 10.5372/1905-7415.0904.424
Sahal G, Bilkay IS (2018) Distribution of clinical isolates of Candida spp. and antifungal susceptibility of high biofilm-forming Candida isolates. Rev Soc Bras Med Trop 51(5):644–650. https://doi.org/10.1590/0037-8682-0136-2018
doi: 10.1590/0037-8682-0136-2018
pubmed: 30304271
Sahal G, Bilkay IS (2014) Multi drug resistance in strong biofilm forming clinical isolates of Staphylococcus epidermidis. Braz J Microbiol 45(2):539–544. https://doi.org/10.1590/s1517-83822014005000042
doi: 10.1590/s1517-83822014005000042
pubmed: 25242939
pmcid: 4166280
Handalishy II, Behery MA, Elkhouly M (2014) Comparative study between probiotic vaginal tampons and oral metronidazole in treatment of bacterial vaginosis. Al-Azhar Assiut Med j 12:185–203
Lewis FMT, Bernstein KT, Aral SO (2017) Vaginal microbiome and its relationship to behavior, sexual health, and sexually transmitted diseases. Obstet Gynecol 129(4):643–654. https://doi.org/10.1097/AOG.0000000000001932
doi: 10.1097/AOG.0000000000001932
pubmed: 28277350
pmcid: 6743080
Freire AD, Custódio AI, Filho JQ, Freitas JC, Gonçalves AK, Cobucci RN (2020) The association between abnormal vaginal flora and cytological evidence of HPV with prematurity in high-risk pregnant women. Gynecol Obstet Reprod Med 26(3):173–178
doi: 10.21613/GORM.2019.928
Tortelli BA, Lewis WG, Allsworth JE, Member-Meneh N, Foster LR, Reno HE, Peipert JF, Fay JC, Lewis AL (2020) Associations between the vaginal microbiome and Candida colonization in women of reproductive age. Am J Obstet Gynecol 222(5):471.e1-471.e9. https://doi.org/10.1016/j.ajog.2019.10.008
doi: 10.1016/j.ajog.2019.10.008
pubmed: 31654610
Curty G, de Carvalho PS, Soares MA (2020) The role of the cervicovaginal microbiome on the genesis and as a biomarker of premalignant cervical intraepithelial neoplasia and invasive cervical cancer. Int J Mol Sci 21(1):222. https://doi.org/10.3390/ijms21010222
doi: 10.3390/ijms21010222
Goldstein EJC, Tyrrell KL, Citron DM (2015) Lactobacillus species: taxonomic complexity and controversial susceptibilities. Clin Infect Dis 60(2):S98–S107. https://doi.org/10.1093/cid/civ072
doi: 10.1093/cid/civ072
pubmed: 25922408
Fan B, Wang C, Song X, Ding X, Wu L, Wu H, Gao X, Borriss R (2018) Bacillus velezensis FZB42 in 2018 the gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol 9:2491. https://doi.org/10.3389/fmicb.2018.02491
doi: 10.3389/fmicb.2018.02491
pubmed: 30386322
pmcid: 6198173
Jiang CH, Liao MJ, Wang HK, Zheng MZ, Xu JJ, Guo JH (2018) Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinerea. Biol Control 12:147–157. https://doi.org/10.1016/j.biocontrol.2018.07.017
doi: 10.1016/j.biocontrol.2018.07.017
Yi Y, Zhang Z, Zhao F, Liu H, Yu L, Zha J, Wang G (2018) Probiotic potential of Bacillus velezensis JW: antimicrobial activity against fish pathogenic bacteria and immune enhancement effects on Carassius auratus. Fish Shellfish Immunol 78:322–330. https://doi.org/10.1016/j.fsi.2018.04.055
doi: 10.1016/j.fsi.2018.04.055
pubmed: 29702236
Pandin C, Darsonval M, Mayeur C, Le Coq D, Aymerich S, Briandet R (2019) Biofilm formation and synthesis of Antimicrobial compounds by the biocontrol agent Bacillus velezensis QST713 in an Agaricus bisporus compost micromodel. Appl Environ Microbiol 85(12):e00327-e419. https://doi.org/10.1128/AEM.00327-19
doi: 10.1128/AEM.00327-19
pubmed: 30979839
pmcid: 6544832
Rabbee MF, Hwang BS, Baek KH (2023) Bacillus velezensis: a beneficial biocontrol agent or facultative phytopathogen for sustainable agriculture. Agronomy 13(3):840. https://doi.org/10.3390/agronomy13030840
doi: 10.3390/agronomy13030840
Yuan H, Shi B, Wang L, Huang T, Zhou Z, Hou H, Tu H (2022) Isolation and characterization of Bacillus velezensis strain P2–1 for biocontrol of apple postharvest decay caused by Botryosphaeria dothidea. Front Microbiol 12:808938. https://doi.org/10.3389/fmicb.2021.808938
doi: 10.3389/fmicb.2021.808938
pubmed: 35058916
pmcid: 8764377
Thurlow CM, Williams MA, Carrias A, Ran C, Newman M, Tweedie J, Allison E, Jescovitch LN, Wilson AE, Terhune JS, Liles MR (2019) Bacillus velezensis AP193 exerts probiotic effects in channel catfish (Ictalurus punctatus) and reduces aquaculture pond eutrophication. Aquaculture 503:347–356. https://doi.org/10.1016/j.aquaculture.2018.11.051
doi: 10.1016/j.aquaculture.2018.11.051
Fooks LJ, Gibson GR (2002) In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol Ecol 9(1):67–75. https://doi.org/10.1016/S0168-6496(01)00197-0
doi: 10.1016/S0168-6496(01)00197-0
Torres-Sánchez A, Pardo-Cacho J, López-Moreno A, Ruiz-Moreno Á, Cerk K, Aguilera M (2021) Antimicrobial effects of potential probiotics of Bacillus spp. isolated from human microbiota: in vitro and in silico methods. Microorganisms 9(8):1615. https://doi.org/10.3390/microorganisms9081615
doi: 10.3390/microorganisms9081615
pubmed: 34442694
pmcid: 8399655
Borah T, Gogoi B, Khataniar A, Gogoi M, Das A, Borah D (2019) Probiotic characterization of indigenous Bacillus velezensis strain DU14 isolated from Apong, a traditionally fermented rice beer of Assam. Biocatal Agric Biotechnol 18:101008. https://doi.org/10.1016/j.bcab.2019.01.046
doi: 10.1016/j.bcab.2019.01.046
Prabhurajeshwar C, Chandrakanth RK (2017) Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances. Biomed J 40(5):270–283. https://doi.org/10.1016/j.bj.2017.06.008
doi: 10.1016/j.bj.2017.06.008
pubmed: 29179882
pmcid: 6138816
Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S, Feeney M, Flynn S, Fitzgerald G, Daly C, Kiely B, O’Sullivan GC, Shanahan F, Collins JK (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73(2):386S-392S. https://doi.org/10.1093/ajcn/73.2.386s
doi: 10.1093/ajcn/73.2.386s
pubmed: 11157346
Mandal S, Puniya AK, Singh K (2006) Effect of alginate concentrations on survival of microencapsulated Lactobacillus casei NCDC-298. Int Dairy J 16(10):1190–1195. https://doi.org/10.1016/j.idairyj.2005.10.005
doi: 10.1016/j.idairyj.2005.10.005
Darmastuti A, Hasan PN, Wikandari R, Utami T, Rahayu ES, Suroto DA (2021) Adhesion properties of Lactobacillus plantarum Dad-13 and Lactobacillus plantarum Mut-7 on Sprague Dawley rat intestine. Microorganisms 9(11):2336. https://doi.org/10.3390/microorganisms9112336
doi: 10.3390/microorganisms9112336
pubmed: 34835461
pmcid: 8625926
Feito J, Contente D, Ponce-Alonso M, Díaz-Formoso L, Araújo C, Peña N, Borrero J, Gómez-Sala B, Del Campo R, Muñoz-Atienza E, Hernández PE, Cintas LM (2022) Draft genome sequence of Lactococcus lactis subsp. cremoris WA2–67: a promising Nisin-producing probiotic strain isolated from the rearing environment of a Spanish rainbow trout (Oncorhynchus mykiss, Walbaum) farm. Microorganisms 10(3):521. https://doi.org/10.3390/microorganisms10030521
doi: 10.3390/microorganisms10030521
pubmed: 35336097
pmcid: 8954438
Kamble A, Naik S, Talathi M, Jadhav D, Pingale S, Kaul-Ghanekar R (2022) Cervicovaginal microbiota isolated from healthy women exhibit probiotic properties and antimicrobial activity against pathogens isolated from cervical cancer patients. Arch Microbiol 204(8):491. https://doi.org/10.1007/s00203-022-03103-5
doi: 10.1007/s00203-022-03103-5
pubmed: 35840844
Ranjit E, Raghubanshi BR, Maskey S, Parajuli P (2018) Prevalence of bacterial vaginosis and its association with risk factors among nonpregnant women: a hospital based study. Int J Microbiol 2018:8349601. https://doi.org/10.1155/2018/8349601
doi: 10.1155/2018/8349601
pubmed: 29692813
pmcid: 5859802
Zhang W, Guo H, Cao C, Li L, Kwok LY, Zhang H, Sun Z (2017) Adaptation of Lactobacillus casei Zhang to gentamycin involves an alkaline shock protein. Front Microbiol 8:2316. https://doi.org/10.3389/fmicb.2017.02316
doi: 10.3389/fmicb.2017.02316
pmcid: 5703869
Mancabelli L, Mancino W, Lugli GA, Argentini C, Longhi G, Milani C, Viappiani A, Anzalone R, Bernasconi S, van Sinderen D, Ventura M, Turroni F (2021) Amoxicillin-clavulanic acid resistance in the genus Bifidobacterium. Appl Environ Microbiol 87(7):e03137-e3220. https://doi.org/10.1128/AEM.03137-20
doi: 10.1128/AEM.03137-20
pubmed: 33483308
pmcid: 8091617
Duche RT, Singh A, Wandhare AG, Sangwan V, Sihag MK, Nwagu TNT, Panwar H, Ezeogu LI (2023) Antibiotic resistance in potential probiotic lactic acid bacteria of fermented foods and human origin from Nigeria. BMC Microbiol 23:142. https://doi.org/10.1186/s12866-023-02883-0
doi: 10.1186/s12866-023-02883-0
pubmed: 37208603
pmcid: 10197481
Ozturk S, Erbas G (2017) Investigation of antibiotic sensivity, isolation and identification of Gardnerella vaginalis collected from Ketem/Aydın Province. Kocatepe Med J 18:61–66
Devi S, Kiesewalter HT, Kovács R, Frisvad JC, Weber T, Larsen TO, Kovács ÁT, Ding L (2019) Depiction of secondary metabolites and antifungal activity of Bacillus velezensis DTU001. Synth Syst Biotechnol 4(3):142–149. https://doi.org/10.1016/j.synbio.2019.08.002
doi: 10.1016/j.synbio.2019.08.002
pubmed: 31508511
pmcid: 6719288