Candida albicans alters the bacterial microbiome of early in vitro oral biofilms

Journal of Oral Microbiology

Volumn 9, Issue 1, 2017, Pages

  Janus, M M ^a,b   Crielaard, W ^a,b   Volgenant, C M C ^a   der Veen, M H van ^a   Brandt, B W ^a,b   Krom, B P ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

Author keywords

Candida albicans; Ecology; In vitro oral biofilms; Oxygen depletion; Red autofluorescence

Indexed keywords

DNA 16S; LACTIC ACID; PROTEINASE;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; AUTOFLUORESCENCE; BACTERIAL MICROBIOME; BIOFILM; CANDIDA ALBICANS; CONTROLLED STUDY; DENTAL CARIES; DNA SEQUENCE; ENZYME ACTIVITY; FUNGUS GROWTH; FUSOBACTERIUM; IN VITRO STUDY; LEPTOTRICHIA; NEISSERIA; NONHUMAN; PERIODONTITIS; PREVOTELLA; ROTHIA; STREPTOCOCCUS; VEILLONELLA;

EID: 85014998801     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.1080/20002297.2016.1270613     Document Type: Article

References (46)

1. Simón-Soro A, Tomás I, Cabrera-Rubio R, et al. Microbial geography of the oral cavity. J Dent Res. 2013;92(7):616-621. doi:10.1177/0022034513488119
2. Zaura E, Keijser BJ, Huse SM, et al. Defining the healthy "core microbiome" of oral microbial communities. BMC Microbiol. 2009;9:259. doi:10.1186/ 1471-2180-9-259
3. Ghannoum MA, Jurevic RJ, Mukherjee PK, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. Plos Pathog. 2010;6(1):e1000713. doi:10.1371/journal.ppat. 1000975
4. Dupuy AK, David MS, Li L, et al. Redefining the human oral mycobiome with improved practices in amplicon-based taxonomy: discovery of Malassezia as a prominent commensal. Plos One. 2014;9(3):e90899. doi:10.1371/journal.pone.0090899
5. WHO. World Health Organization: oral health fact sheet No318. WHO Media Centre; 2012. www.who. int/mediacentre/factsheets/fs318/en/
6. Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res. 1994;8(2):263-271.
7. Marsh PD. Are dental diseases examples of ecological catastrophes? Microbiology. 2003;149(Pt 2):279-294. doi:10.1099/mic.0.26082-0
8. Raja M, Hannan A, Ali K. Association of oral candidal carriage with dental caries in children. Caries Res. 2010;44(3):272-276. doi:10.1159/000314675
9. Odds FC. Candida and candidosis. London: Bailliere Tindall; 1988.
10. Krom BP, Kidwai S, Ten Cate JM. Candida and other fungal species: forgotten players of healthy oral microbiota. J Dent Res. 2014;93(5):445-451. doi:10.1177/ 0022034514521814
11. Silverman RJ, Nobbs AH, Vickerman MM, et al. Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun. 2010;78(11):4644-4652. doi:10.1128/ IAI.00685-10
12. Falsetta ML, Klein MI, Colonne PM, et al. Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo. Infect Immun. 2014;82(5):1968-1981. doi:10.1128/IAI.00087-14
13. Bachtiar EW, Bachtiar BM, Jarosz LM, et al. AI-2 of Aggregatibacter actinomycetemcomitans inhibits Candida albicans biofilm formation. Front Cell Infectmicrobiol. 2014;4:94.
14. Jarosz LM, Deng DM, van der Mei HC, et al. Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot Cell. 2009;8(11):1658-1664. doi:10.1128/EC.00070- 09
15. Willems M, Kos K, Jabra-Rizk MA, et al. Candida albicans in oral biofilms could prevent caries. Pathog Dis. 2016;74:ftw039. doi:10.1093/femspd/ftw039
16. Metwalli KH, Khan SA, Krom BP, et al. Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. Plos Pathog. 2013;9(10):e1003616. doi:10.1371/journal.ppat.1003616
17. Vylkova S, Carman AJ, Danhof HA, et al. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio. 2011;2 (3):e00055-11. doi:10.1128/mBio.00055-11
18. Janus MM, Keijser BJ, Bikker FJ, et al. In vitro phenotypic differentiation towards commensal and pathogenic oral biofilms. Biofouling. 2015;31(6):503-510. doi:10.1080/08927014.2015.1067887
19. Fonzi WA, Irwin MY. Isogenic strain construction and gene mapping in Candida albicans. Genetics. 1993;134(3):717-728.
20. Exterkate RA, Crielaard W, Ten Cate JM. Different response to amine fluoride by Streptococcus mutans and polymicrobial biofilms in a novel high-throughput active attachment model. Caries Res. 2010;44 (4):372-379. doi:10.1159/000316541
21. Vollmer T, Störmer M, Kleesiek K, et al. Evaluation of novel broad-range real-time PCR assay for rapid detection of human pathogenic fungi in various clinical specimens. J Clin Microbiol. 2008;46(6):1919-1926. doi:10.1128/JCM.02178-07
22. Geddes DA. Acids produced by human dental plaque metabolism in situ. Caries Res. 1975;9(2):98-109.
23. van Loveren C, Buijs JF, Ten Cate JM. The effect of triclosan toothpaste on enamel demineralization in a bacterial demineralization model. J Antimicrob Chemother. 2000;45(2):153-158.
24. Kaman WE, Galassi F, de Soet JJ, et al. Highly specific protease-based approach for detection of porphyromonas gingivalis in diagnosis of periodontitis. J Clin Microbiol. 2012;50(1):104-112. doi:10.1128/ JCM.05313-11
25. Cummings RT, Salowe SP, Cunningham BR, et al. A peptide-based fluorescence resonance energy transfer assay for Bacillus anthracis lethal factor protease. Proc Natl Acad Sci U S A. 2002;99(10):6603-6606. doi:10.1073/pnas.062171599
26. Kim Y-S, Lee E-S, Kwon H-K, et al. Monitoring the maturation process of a dental microcosm biofilm using the Quantitative Light-induced Fluorescence- Digital (QLF-D). J Dent. 2014;42(6):691-696. doi:10.1016/j.jdent.2014.03.006
27. Volgenant CM, Hoogenkamp MA, Buijs MJ, et al. Red fluorescent biofilm: the thick, the old, and the cariogenic. J Oral Microbiol. 2016;8:30346. doi:10.3402/ jom.v8.30346
28. van der Veen MH, Volgenant CM, Keijser B, et al. Dynamics of red fluorescent dental plaque during experimental gingivitis-A cohort study. J Dent. 2016;48:71-76. doi:10.1016/j.jdent.2016.02.010
29. Koenig K, Hibst R, Meyer H, et al., editors. Laserinduced autofluorescence of carious regions of human teeth and caries-involved bacteria. Europto biomedical optics' 93. International Society for Optics and Photonics; 1993. doi:10.1117/12.166180
30. O'Donnell LE, Robertson D, Nile CJ, et al. The oral microbiome of denture wearers is influenced by levels of natural dentition. Plos One. 2015;10(9):e0137717. doi:10.1371/journal.pone.0137717
31. Koopman JE, Buijs MJ, Brandt BW, et al. Nitrate and the origin of saliva influence composition and short chain fatty acid production of oral microcosms. Microb Ecol. 2016;72:479-492. doi:10.1007/s00248- 016-0775-z
32. Hammer Ø, Harper D, Ryan P. PASTPAlaeontological STatistics, ver. 1.89. Palaeontol Electron. 2001;4(1):1-9.
33. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi:10.1186/gb-2011-12-10- r102
34. Dumitru R, Hornby JM, Nickerson KW. Defined anaerobic growth medium for studying Candida albicans basic biology and resistance to eight antifungal drugs. Antimicrob Agents Chemother. 2004;48(7):2350-2354. doi:10.1128/AAC.48.7.2350-2354.2004
35. Bahn Y-S, Mühlschlegel FA. CO2 sensing in fungi and beyond. Curr Opin Microbiol. 2006;9(6):572-578. doi:10.1016/j.mib.2006.09.003
36. Klinke T, Guggenheim B, Klimm W, et al. Dental caries in rats associated with Candida albicans. Caries Res. 2011;45(2):100-106. doi:10.1159/000324809
37. Kolenbrander PE, Palmer RJ Jr., Rickard AH, et al. Bacterial interactions and successions during plaque development. Periodontol 2000. 2006;42:47-79. doi:10.1111/j.1600-0757.2006.00187.x
38. Distler W, Kröncke A. Acid formation by mixed cultures of cariogenic strains of Streptococcus mutans and Veillonella alcalescens. Arch Oral Biol. 1980;25 (10):655-658.
39. Brand A, Barnes JD,Mackenzie KS, et al. Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa. FEMS Microbiol Lett. 2008;287(1):48-55. doi:10.1111/ j.1574-6968.2008.01301.x
40. Peters BM, Ovchinnikova ES, Krom BP, et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology. 2012;158(Pt 12):2975-2986. doi:10.1099/mic.0.062109-0
41. Fox EP, Cowley ES, Nobile CJ, et al. Anaerobic bacteria grow within Candida albicans biofilms and induce biofilm formation in suspension cultures. Curr Biol. 2014;24(20):2411-2416. doi:10.1016/j.cub.2014.08.057
42. Wesolowski J, Hassan RY, Hodde S, et al. Sensing of oxygen in microtiter plates: a novel tool for screening drugs against pathogenic yeasts. Anal Bioanal Chem. 2008;391(5):1731-1737. doi:10.1007/s00216-008- 1947-6
43. Johansson I, Witkowska E, Kaveh B, et al. The microbiome in populations with a low and high prevalence of caries. J Dent Res. 2016;95(1):80-86. doi:10.1177/ 0022034515609554
44. Nadkarni MA, Caldon CE, Chhour K-L, et al. Carious dentine provides a habitat for a complex array of novel Prevotella-like bacteria. J Clin Microbiol. 2004;42 (11):5238-5244. doi:10.1128/JCM.42.11.5238-5244.2004
45. Gomar-Vercher S, Cabrera-Rubio R, Mira A, et al. Relationship of children's salivary microbiota with their caries status: a pyrosequencing study. Clin Oral Investig. 2014;18(9):2087-2094. doi:10.1007/s00784- 014-1200-y
46. Kara D, Luppens SB, Cate JM. Differences between single- and dual-species biofilms of Streptococcus mutans and Veillonella parvula in growth, acidogenicity and susceptibility to chlorhexidine. Eur J Oral Sci. 2006;114 (1):58-63. doi:10.1111/j.1600-0722.2006.00262.x