In the last half-decade or so, interest in the bacterial part of the human microbiome and its role in maintaining health have received considerable attention. Since 2009, over 300 publications have appeared describing the oral bacterial microbiome. Strikingly, fungi in the oral cavity have been studied exclusively in relation to pathologies. However, little to nothing is known about a role of fungi in establishing and maintaining a healthy oral ecology. In a healthy ecology, balance is maintained by the combined positive and negative influences between and among its members. Interactions between fungi and bacteria occur primarily at a physical and chemical level. Physical interactions are represented by (co-)adhesion and repulsion (exclusion), while chemical interactions include metabolic dependencies, quorum-sensing, and the production of antimicrobial agents. Information obtained from oral model systems and also from studies on the role of fungi in gastro-intestinal ecology indicates that fungi influence bacterial behavior through these different interactions. This review describes our current knowledge of the interactions between fungi and bacteria and aims to illustrate that further research is required to establish the role of fungi in maintaining a healthy oral cavity.
BizzarroSLoosBGLaineMLCrielaardWZauraE (2013). Subgingival microbiome in smokers and non-smokers in periodontitis: an exploratory study using traditional targeted techniques and a next-generation sequencing. J Clin Periodontol40:483-492.
4.
BjarnsholtTTolker-NielsenTHøibyNGivskovM (2010). Interference of Pseudomonas aeruginosa signalling and biofilm formation for infection control. Expert Rev Mol Med12:e11.
5.
BrandABarnesJDMackenzieKSOddsFCGowNA (2008). Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa. FEMS Microbiol Lett287:48-55.
6.
CephasKDKimJMathaiRABarryKADowdSEMelineBS. (2011). Comparative analysis of salivary bacterial microbiome diversity in edentulous infants and their mothers or primary care givers using pyrosequencing. PloS one6:e23503.
7.
CrielaardWZauraESchullerAAHuseSMMontijnRCKeijserBJ (2011). Exploring the oral microbiota of children at various developmental stages of their dentition in the relation to their oral health. BMC Med Genomics4:22.
8.
CuginiCCalfeeMWFarrowJM3rdMoralesDKPesciECHoganDA (2007). Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol65:896-906.
9.
CuginiCMoralesDKHoganDA (2010). Candida albicans-produced farnesol stimulates Pseudomonas quinolone signal production in LasR-defective Pseudomonas aeruginosa strains. Microbiology156(Pt 10):3096-3107.
10.
DewhirstFEChenTIzardJPasterBJTannerACYuWH. (2010). The human oral microbiome. J Bacteriol192:5002-5017.
11.
Erb DownwardJRFalkowskiNRMasonKLMuragliaRHuffnagleGB (2013). Modulation of post-antibiotic bacterial community reassembly and host response byCandida albicans. Sci Rep3:2191.
12.
FalsettaMLKleinMILemosJASilvaBBAgidiSScott-AnneKK. (2012). Novel antibiofilm chemotherapy targets exopolysaccharide synthesis and stress tolerance in Streptococcus mutans to modulate virulence expression in vivo. Antimicrob Agents Chemother56:6201-6211.
FolkeCCarpenterSWalkerBSchefferMElmqvistTGundersonL. (2004). Regime shifts, resilience, and biodiversity in ecosystem management. Ann Rev Ecol Evol Systematics35:557-581.
15.
GhannoumMAJurevicRJMukherjeePKCuiFSikaroodiMNaqviA. (2010). Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog6:e1000713.
16.
GrossELLeysEJGasparovichSRFirestoneNDSchwartzbaumJAJaniesDA. (2010). Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol48:4121-4128.
17.
GrossELBeallCJKutschSRFirestoneNDLeysEJGriffenAL (2012). Beyond Streptococcus mutans: dental caries onset linked to multiple species by 16S rRNA community analysis. PloS one7:e47722.
18.
HarriottMMNoverrMC (2009). Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother53:3914-3922.
19.
HoganDAKolterR (2002). Pseudomonas-Candida interactions: an ecological role for virulence factors. Science296:2229-2232.
HornbyJMJensenECLisecADTastoJJJahnkeBShoemakerR. (2001). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol67:2982-2992.
22.
Human Microbiome Project Consortium (2012). Structure, function and diversity of the healthy human microbiome. Nature486:207-214.
23.
HuseSMYeYZhouYFodorAA (2012). A core human microbiome as viewed through 16S rRNA sequence clusters. PloS one7:e34242.
24.
JangYJChoiYJLeeSHJunHKChoiBK (2013). Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Arch Oral Biol58:17-27.
JaroszLMOvchinnikovaESMeijlerMMKromBP (2011). Microbial spy games and host response: roles of a Pseudomonas aeruginosa small molecule in communication with other species. PLoS Pathog7:e1002312.
27.
JenkinsonHF (2011). Beyond the oral microbiome. Environ Microbiol13:3077-3087.
28.
JenkinsonHFLamontRJ (2005). Oral microbial communities in sickness and in health. Trends Microbiol13:589-595.
29.
JoynerPMLiuJZhangZMerrittJQiFCichewiczRH (2010). Mutanobactin A from the human oral pathogen Streptococcus mutans is a cross-kingdom regulator of the yeast-mycelium transition. Organic & biomolecular chemistry8:5486-5489.
30.
KanasiEDewhirstFEChalmersNIKentRJrMooreAHughesCV. (2010). Clonal analysis of the microbiota of severe early childhood caries. Caries Res44:485-497.
31.
KeijserBJZauraEHuseSMvan der VossenJMSchurenFHMontijnRC. (2008). Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res87:1016-1020.
32.
KimJSudberyP (2011). Candida albicans, a major human fungal pathogen. J Microbiol49:171-177.
33.
KlinkeTGuggenheimBKlimmWThurnheerT (2011). Dental caries in rats associated with Candida albicans. Caries Res45:100-106.
34.
KolenbranderPE (2011). Multispecies communities: interspecies interactions influence growth on saliva as sole nutritional source. Int J Oral Sci3:49-54.
35.
KolenbranderPEPalmerRJJrPeriasamySJakubovicsNS (2010). Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol8:471-480.
36.
KönönenEJousimies-SomerHBrykAKilpTKilianM (2002). Establishment of streptococci in the upper respiratory tract: longitudinal changes in the mouth and nasopharynx up to 2 years of age. J Med Microbiol51:723-730.
37.
KraneveldEABuijsMJBonderMJVisserMKeijserBJCrielaardW. (2012). The relation between oral Candida load and bacterial microbiome profiles in Dutch older adults. PloS one7:e42770.
38.
LazarevicVWhitesonKHuseSHernandezDFarinelliLOsteråsM. (2009). Metagenomic study of the oral microbiota by Illumina high-throughput sequencing. J Microbiol Methods79:266-271.
39.
MarshPD (2012). Contemporary perspective on plaque control. Br Dent J212:601-606.
40.
MasonKLErb DownwardJRFalkowskiNRYoungVBKaoJYHuffnagleGB (2012a). Interplay between the gastric bacterial microbiota and Candida albicans during postantibiotic recolonization and gastritis. Infect Immun80:150-158.
41.
MasonKLErb DownwardJRMasonKDFalkowskiNREatonKAKaoJY. (2012b). Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun80:3371-3380.
42.
MetwalliKHKhanSAKromBPJabra-RizkMA (2013). Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. PLoS Pathog9:e1003616.
43.
MoralesDKHoganDA (2010). Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog6:e1000886.
44.
NaglikJRTangSXMoyesDL (2013). Oral colonization of fungi. Curr Fungal Infection Rep7:152-159.
45.
NobbsAHVickermanMMJenkinsonHF (2010). Heterologous expression of Candida albicans cell wall-associated adhesins in Saccharomyces cerevisiae reveals differential specificities in adherence and biofilm formation and in binding oral Streptococcus gordonii. Eukaryot Cell9:1622-1634.
46.
OvchinnikovaESKromBPvan der MeiHCBusscherHJ (2012). Force microscopic and thermodynamic analysis of the adhesion between Pseudomonas aeruginosa and Candida albicans. Soft Matter8:6454-6461.
47.
OvchinnikovaESKromBPHarapanahalliAKBusscherHJvan der MeiHC (2013). Surface thermodynamic and adhesion force evaluation of the role of chitin-binding protein in the physical interaction between Pseudomonas aeruginosa and Candida albicans. Langmuir29:4823-4829.
48.
Pereira-CenciTDengDMKraneveldEAMandersEMDel Bel CuryAAten CateJM. (2008). The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch Oral Biol53:755-764.
49.
PetersBMOvchinnikovaESKromBPSchlechtLMZhouHHoyerLL. (2012). Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology158(Pt 12):2975-2986.
50.
RelmanDA (2012). The human microbiome: ecosystem resilience and health. Nutr Rev70 (Suppl 1):S2-9.
51.
RickardAHGilbertPHighNJKolenbranderPEHandleyPS (2003). Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol11:94-100.
52.
RubyJGoldnerM (2007). Nature of symbiosis in oral disease. J Dent Res86:8-11.
53.
RudneyJDChenRZhangG (2005). Streptococci dominate the diverse flora within buccal cells. J Dent Res84:1165-1171.
54.
SilvermanRJNobbsAHVickermanMMBarbourMEJenkinsonHF (2010). Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun78:4644-4652.
55.
Simon-SoroATomasICabrera-RubioRCatalanMDNyvadBMiraA (2013). Microbial geography of the oral cavity. J Dent Res92:616-621.
56.
SmeeD (2012). Species with a large impact on community structure. Nature Education Knowledge3(10):40.
57.
WeerasekeraMMSissonsCHWongLAndersonSHolmesARCannonRD (2013). Use of denaturing gradient gel electrophoresis for the identification of mixed oral yeasts in human saliva. J Med Microbiol62(Pt 2):319-330.
58.
WilliamsDWJordanRPWeiXQAlvesCTWiseMPWilsonMJ. (2013). Interactions of Candida albicans with host epithelial surfaces. J Oral Microbiol5:22434.
59.
WrightCJBurnsLHJackAABackCRDuttonLCNobbsAH. (2013). Microbial interactions in building of communities. Mol Oral Microbiol28:83-101.
60.
ZarcoMFVessTJGinsburgGS (2012). The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis18:109-120.
61.
ZauraEKeijserBJHuseSMCrielaardW (2009). Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol9:259.
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