Oral Mycobiome Analysis of HIV-Infected Patients: Identification of as an Antagonist of Opportunistic Fungi
Oral microbiota contribute to health and disease, and their disruption may influence the course of oral diseases like oral candidiasis. Here we identify the core oral mycobiome (COM) and core oral bacteriome (COB) in HIV-infected and uninfected individuals, and demonstrate that the COM differs between these two groups. Decrease in abundance of Pichia (a resident oral fungus) in uninfected individuals coincided with increase in abundance of Candida, suggesting an antagonistic relationship. In vitro testing showed that Pichia spent medium (PSM) inhibits growth of pathogenic fungi; these findings were validated in an experimental mouse modal of oral candidiasis. The mechanism by which Pichia antagonizes Candida involves nutrient competition and secretory factor/s that inhibit the latter's ability to adhere, germinate, and form biofilms. This study is the first to characterize the mycobiome and the bacteriome in the oral cavity of HIV infected patients, and provides the first evidence that a fungus present in the same host microenvironment antagonizes Candida and identifies potential novel antifungal approach.
Vyšlo v časopise:
Oral Mycobiome Analysis of HIV-Infected Patients: Identification of as an Antagonist of Opportunistic Fungi. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003996
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003996
Souhrn
Oral microbiota contribute to health and disease, and their disruption may influence the course of oral diseases like oral candidiasis. Here we identify the core oral mycobiome (COM) and core oral bacteriome (COB) in HIV-infected and uninfected individuals, and demonstrate that the COM differs between these two groups. Decrease in abundance of Pichia (a resident oral fungus) in uninfected individuals coincided with increase in abundance of Candida, suggesting an antagonistic relationship. In vitro testing showed that Pichia spent medium (PSM) inhibits growth of pathogenic fungi; these findings were validated in an experimental mouse modal of oral candidiasis. The mechanism by which Pichia antagonizes Candida involves nutrient competition and secretory factor/s that inhibit the latter's ability to adhere, germinate, and form biofilms. This study is the first to characterize the mycobiome and the bacteriome in the oral cavity of HIV infected patients, and provides the first evidence that a fungus present in the same host microenvironment antagonizes Candida and identifies potential novel antifungal approach.
Zdroje
1. JenkinsonHF, LamontRJ (2005) Oral microbial communities in sickness and in health. Trends Microbiol 13: 589–595.
2. PattonLL, PhelanJA, Ramos-GomezFJ, NittayanantaW, ShiboskiCH, et al. (2002) Prevalence and classification of HIV-associated oral lesions. Oral Dis 8: 98–109.
3. ChattopadhyayA, CaplanDJ, SladeGD, ShugarsDC, TienHC, et al. (2005) Risk indicators for oral candidiasis and oral hairy leukoplakia in HIV-infected adults. Community Dent Oral Epidemiol 33: 35–44.
4. Koletar SL, Smurzynski M, Wu K, Collier AC, Bosch RJ, et al.. AIDS-defining illnesses occurring in treatment-experienced HIV-1-infected persons followed in the ACTG Longitudinal Linked Randomized Trials (ALLRT) study [Abstract 1017]. In Proceedings of the 15th Conference on Retroviruses & Opportunistic Infections; February 3–6, 2008; Boston, MA. Available: http://retroconference.org/. Accessed 2/3/13.
5. ThompsonGR3rd, PatelPK, KirkpatrickWR, WestbrookSD, BergD, et al. (2010) Oropharyngeal candidiasis in the era of antiretroviral therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109: 488–495.
6. PatelPK, ErlandsenJE, KirkpatrickWR, BergDK, WestbrookSD, et al. (2012) The Changing Epidemiology of Oropharyngeal Candidiasis in Patients with HIV/AIDS in the Era of Antiretroviral Therapy. AIDS Res Treat 2012: 262471.
7. KinrossJM, DarziAW, NicholsonJK (2011) Gut microbiome-host interactions in health and disease. Genome Med 3: 14.
8. NelsonKE, WeinstockGM, HighlanderSK, WorleyKC, CreasyHH, et al. (2010) A catalog of reference genomes from the human microbiome. Science 328: 994–999.
9. GriceEA, KongHH, ConlanS, DemingCB, DavisJ, et al. (2009) Topographical and temporal diversity of the human skin microbiome. Science 324: 1190–1192.
10. HuseSM, YeY, ZhouY, FodorAA (2012) A Core Human Microbiome as Viewed through 16S rRNA Sequence Clusters. PLoS ONE 7: e34242.
11. ClementeJC, UrsellLK, ParfreyLW, KnightR (2012) The Impact of the Gut Microbiota on Human Health: An Integrative View. Cell 148: 1258–1270.
12. AasJA, BarbutoSM, AlpagotT, OlsenI, DewhirstFE, et al. (2007) Subgingival plaque microbiota in HIV positive patients. Journal of Clinical Periodontology 34: 189–195.
13. IlievID, FunariVA, TaylorKD, NguyenQ, ReyesCN, et al. (2012) Interactions Between Commensal Fungi and the C-Type Lectin Receptor Dectin-1 Influence Colitis. Science 336: 1314–1317.
14. GhannoumMA, JurevicRJ, MukherjeePK, CuiF, SikaroodiM, et al. (2010) Characterization of the Oral Fungal Microbiome (Mycobiome) in Healthy Individuals. PLoS Pathogens 6: e1000713.
15. PelegAY, HoganDA, MylonakisE (2010) Medically important bacterial-fungal interactions. Nat Rev Microbiol 8: 340–349.
16. LandlingerC, BaskovaL, PreunerS, WillingerB, BuchtaV, et al. (2008) Identification of fungal species by fragment length analysis of the internally transcribed spacer 2 region. Eur J Clin Microbiol Infect Dis 28 (6) 613–22.
17. BormanAM, LintonCJ, MilesSJ, JohnsonEM (2008) Molecular identification of pathogenic fungi. Journal of Antimicrobial Chemotherapy 61: i7–12.
18. GillevetP, SikaroodiM, KeshavarzianA, MutluEA (2010) Quantitative assessment of the human gut microbiome using multitag pyrosequencing. Chem Biodivers 7: 1065–1075.
19. ChakravortyS, HelbD, BurdayM, ConnellN, AllandD (2007) A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. Journal of Microbiological Methods 69: 330–339.
20. SpearGT, SikaroodiM, ZariffardMR, LandayAL, FrenchAL, et al. (2008) Comparison of the diversity of the vaginal microbiota in HIV-infected and HIV-uninfected women with or without bacterial vaginosis. J Infect Dis 198: 1131–1140.
21. Gillevet PM, inventor; BioSpherex LLC, assignee (2013 December 10) Multitag Sequencing and Ecogenomic Analysis. United States Patent 8,603,749.
22. RomanelliAM, SuttonDA, ThompsonEH, RinaldiMG, WickesBL (2010) Sequence-based identification of filamentous basidiomycetous fungi from clinical specimens: a cautionary note. J Clin Microbiol 48: 741–752.
23. CormackBP, BertramG, EgertonM, GowNA, FalkowS, et al. (1997) Yeast-enhanced green fluorescent protein (yEGFP) a reporter of gene expression in Candida albicans. Microbiology 143: 303–311.
24. SwindellK, LattifAA, ChandraJ, MukherjeePK, GhannoumMA (2009) Parenteral Lipid Emulsion Induces Germination of Candida albicans and Increases Biofilm Formation on Medical Catheter Surfaces. J Infect Dis 200: 473–480.
25. KuhnDM, MukherjeePK, ClarkeTA, PujolC, ChandraJ, et al. (2004) Candida parapsilosis characterization in an outbreak setting. Emerging Infectious Diseases 10: 1074–1081.
26. ChandraJ, MukherjeePK, GhannoumMA (2008) In vitro growth and analysis of Candida biofilms. Nature Protocols 3: 1909–1924.
27. ChandraJ, KuhnDM, MukherjeePK, HoyerLL, McCormickT, et al. (2001) Biofilm formation by the fungal pathogen Candida albicans - development, architecture and drug resistance. Journal of Bacteriology 183: 5385–5394.
28. ChandraJ, MukherjeePK, LeidichSD, FaddoulFF, HoyerLL, et al. (2001) Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. Journal of Dental Research 80: 903–908.
29. PienaarED, YoungT, HolmesH (2010) Interventions for the prevention and management of oropharyngeal candidiasis associated with HIV infection in adults and children. Cochrane Database of Systematic Reviews 11: CD003940.
30. HiseAG, TomalkaJ, GanesanS, PatelK, HallBA, et al. (2009) An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5: 487–497.
31. TangN, LiuL, KangK, MukherjeePK, TakaharaM, et al. (2004) Inhibition of monocytic interleukin-12 production by Candida albicans via selective activation of ERK mitogen-activated protein kinase. Infection and Immunity 72: 2513–2520.
32. GhannoumMA, MukherjeePK, JurevicRJ, RetuertoM, BrownRE, et al. (2011) Metabolomics Reveals Differential Levels of Oral Metabolites in HIV-Infected Patients: Toward Novel Diagnostic Targets. Omics 17: 5–15.
33. CaporasoJG, KuczynskiJ, StombaughJ, BittingerK, BushmanFD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
34. R Core Team (2013) R: A language and environment for statistical computing. Available http://www.R-project.org. Accessed 2 February 2013.
35. Revelle W (2013) psych: procedures for personality and psychological research. Available http://CRAN.R-project.org/package=psych Version = 1.3.10. Accessed 20 December 2013.
36. NoktaM (2008) Oral manifestations associated with HIV infection. Curr HIV/AIDS Rep 5: 5–12.
37. SchislerD, KurtzmanC, BothastR, SliningerP (1995) Evaluation of yeasts for biological control of Fusarium dry rot of potatoes. American Potato Journal 72: 339–353.
38. StarmerWT, GanterPF, PhaffHJ (1986) Quantum and continuous evolution of DNA base composition in the yeast genus Pichia. Evolution 40: 1263–1274.
39. Golubev W (2006) Antagonistic interactions among yeasts. Biodiversity and Ecophysiology of Yeasts: Springer. pp. 197–219.
40. AntunesJ, AguiarC (2012) Search for killer phenotypes with potential for biological control. Annals of microbiology 62: 427–433.
41. DruveforsUA, SchnurerJ (2005) Mold-inhibitory activity of different yeast species during airtight storage of wheat grain. FEMS Yeast Res 5: 373–378.
42. JungPP, FriedrichA, SoucietJL, LouisV, PotierS, et al. (2010) Complete mitochondrial genome sequence of the yeast Pichia farinosa and comparative analysis of closely related species. Curr Genet 56: 507–515.
43. WalkerGM (2010) Pichia anomala: cell physiology and biotechnology relative to other yeasts. Antonie Van Leeuwenhoek 99 (1) 25–34.
44. EladY (2003) Biocontrol of foliar pathogens: mechanisms and application. Commun Agric Appl Biol Sci 68: 17–24.
45. CaoS, YuanY, HuZ, ZhengY (2010) Combination of Pichia membranifaciens and ammonium molybdate for controlling blue mould caused by Penicillium expansum in peach fruit. Int J Food Microbiol 141: 173–176.
46. SantosA, San MauroM, BravoE, MarquinaD (2009) PMKT2, a new killer toxin from Pichia membranifaciens, and its promising biotechnological properties for control of the spoilage yeast Brettanomyces bruxellensis. Microbiology 155: 624–634.
47. OlstorpeM, PassothV (2010) Pichia anomala in grain biopreservation. Antonie Van Leeuwenhoek 99 (1) 57–62.
48. KaganBL (1983) Mode of action of yeast killer toxins: channel formation in lipid bilayer membranes. Nature 302: 709–711.
49. İzgüF, AltınbayD, AcunT (2006) Killer toxin of Pichia anomala NCYC 432; purification, characterization and its exo-β-1,3-glucanase activity. Enzyme and Microbial Technology 39: 669–676.
50. CaoS, ZhengY, TangS, WangK (2008) Improved control of anthracnose rot in loquat fruit by a combination treatment of Pichia membranifaciens with CaCl(2). Int J Food Microbiol 126: 216–220.
51. DruveforsUA, PassothV, SchnurerJ (2005) Nutrient effects on biocontrol of Penicillium roqueforti by Pichia anomala J121 during airtight storage of wheat. Appl Environ Microbiol 71: 1865–1869.
52. XuXB, TianSP (2008) Reducing oxidative stress in sweet cherry fruit by Pichia membranaefaciens: a possible mode of action against Penicillium expansum. J Appl Microbiol 105: 1170–1177.
53. ZhaoJ, MouY, ShanT, LiY, ZhouL, et al. (2010) Antimicrobial metabolites from the endophytic fungus Pichia guilliermondii isolated from Paris polyphylla var. yunnanensis. Molecules 15: 7961–7970.
54. JijakliMH, LepoivreP (1998) Characterization of an Exo-beta-1,3-Glucanase Produced by Pichia anomala Strain K, Antagonist of Botrytis cinerea on Apples. Phytopathology 88: 335–343.
55. DrobyS, HofsteinR, WilsonCL, WisniewskiM, FridlenderB, et al. (1993) Pilot Testing of Pichia guilliermondii: A Biocontrol Agent of Postharvest Diseases of Citrus Fruit. Biological Control 3: 47–52.
56. DrobyS, WisniewskiME, CohenL, WeissB, TouitouD, et al. (1997) Influence of CaCl(2) on Penicillium digitatum, Grapefruit Peel Tissue, and Biocontrol Activity of Pichia guilliermondii. Phytopathology 87: 310–315.
57. GiobbeS, MarcedduS, SchermB, ZaraG, MazzarelloVL, et al. (2007) The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res 7: 1389–1398.
58. KumamotoCA, VincesMD (2005) Alternative Candida albicans lifestyles: Growth on Surfaces. Annual Review of Microbiology 59: 113–133.
59. ChandraJ, MukherjeePK, GhannoumMA (2011) Candida Biofilms Associated with CVC and Medical Devices. Mycoses 55: 46–57.
60. ChandraJ, MukherjeePK, GhannoumMA (2010) Fungal Biofilms in the Clinical Lab Setting. Current Reports in Fungal Infection 4: 137–144.
61. ConlanS, KongHH, SegreJA (2012) Species-level analysis of DNA sequence data from the NIH Human Microbiome Project. PLoS One 7: e47075.
62. LiK, BihanM, YoosephS, MetheBA (2012) Analyses of the microbial diversity across the human microbiome. PLoS One 7: e32118.
63. ZarcoMF, VessTJ, GinsburgGS (2012) The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis 18: 109–120.
64. ZauraE, KeijserBJ, HuseSM, CrielaardW (2009) Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 9: 259.
65. HoganDA, KolterR (2002) Pseudomonas - Candida interactions: an ecological role for virulence factors. Science 296: 2229–2232.
66. AzoulayE, TimsitJ-F, TaffletM, de LassenceA, DarmonM, et al. (2006) Candida Colonization of the Respiratory Tract and Subsequent Pseudomonas Ventilator-Associated Pneumonia. Chest 129: 110–117.
67. NseirS, JozefowiczE, CavestriB, SendidB, Di PompeoC, et al. (2007) Impact of antifungal treatment on Candida-Pseudomonas interaction: a preliminary retrospective case-control study. Intensive Care Med 33: 137–142.
68. DyessDL, GarrisonRN, FryDE (1985) Candida sepsis. Implications of polymicrobial blood-borne infection. ArchSurg 120: 345–348.
69. NavazeshM, MulliganR, PogodaJ, GreenspanD, AlvesM, et al. (2005) The effect of HAART on salivary microbiota in the Women's Interagency HIV Study (WIHS). Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100: 701–708.
70. WorkmanSN, BeenFE, CrawfordSR, LavoieMC (2008) Bacteriocin-like inhibitory substances from Campylobacter spp. Antonie Van Leeuwenhoek 93: 435–436.
71. DupontPF (1995) Candida albicans, the opportunist. A cellular and molecular perspective. JAmPodiatrMedAssoc 85: 104–115.
72. MartinMV, CraigGT, LambDJ (1984) An investigation of the role of true hypha production in the pathogenesis of experimental oral candidosis. Sabouraudia 22: 471–476.
73. CannonRD, HolmesAR, MasonAB, MonkBC (1995) Oral Candida: clearance, colonization, or candidiasis? JDentRes 74: 1152–1161.
74. SamaranayakeYH, WuPC, SamaranayakeLP, SoM, YuenKY (1994) Adhesion and colonisation of Candida krusei on host surfaces. JMedMicrobiol 41: 250–258.
75. De BernardisF, BoccaneraM, RainaldiL, GuerraCE, QuintiI, et al. (1992) The secretion of aspartyl proteinase, a virulence enzyme, by isolates of Candida albicans from the oral cavity of HIV-infected subjects. EurJEpidemiol 8: 362–367.
76. SardiJC, DuqueC, HoflingJF, GoncalvesRB (2012) Genetic and phenotypic evaluation of Candida albicans strains isolated from subgingival biofilm of diabetic patients with chronic periodontitis. Med Mycol 50: 467–475.
77. GhannoumMA, Abu-ElteenKH (1990) Pathogenicity determinants of Candida. Mycoses 33: 265–282.
78. GhannoumMA (2000) Potential role of phospholipases in virulence and fungal pathogenesis. Clinical Microbiology Reviews 13: 122–143.
79. RichardsonMD, SmithH (1981) Production of germ tubes by virulent and attenuated strains of Candida albicans. J Infect Dis 144: 565–569.
80. RestucciaC, GiusinoF, LicciardelloF, RandazzoC, CaggiaC, et al. (2006) Biological control of peach fungal pathogens by commercial products and indigenous yeasts. J Food Prot 69: 2465–2470.
81. SantosA, MarquinaD (2004) Ion channel activity by Pichia membranifaciens killer toxin. Yeast 21: 151–162.
82. FredlundE, BrobergA, BoysenME, KenneL, SchnurerJ (2004) Metabolite profiles of the biocontrol yeast Pichia anomala J121 grown under oxygen limitation. Appl Microbiol Biotechnol 64: 403–409.
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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