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Cited by 68Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

One population, multiple lifestyles: Commensalism and pathogenesis in the human mycobiome

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Proctor, Diana M., Drummond, Rebecca A., Lionakis, Michail S., Segre, Julia A.·2023·Cell Host & Microbe
DOI 10.1016/j.chom.2023.02.010PMC PMC10155287
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Abstract

Candida auris and Candida albicans can result in invasive fungal diseases. And yet, these species can stably and asymptomatically colonize human skin and gastrointestinal tracts. To consider these disparate microbial lifestyles, we first review factors shown to influence the underlying microbiome. Structured by the damage response framework, we then consider the molecular mechanisms deployed by C. albicans to switch between commensal and pathogenic lifestyles. Next, we explore this framework with C. auris to highlight how host physiology, immunity, and/or antibiotic receipt are associated with progression from colonization to infection. While treatment with antibiotics increases the risk that an individual will succumb to invasive candidiasis, the underlying mechanisms remain unclear. Here, we describe several hypotheses that may explain this phenomenon. We conclude by highlighting future directions integrating genomics with immunology to advance our understanding of invasive candidiasis and human fungal disease.

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  • C. auris has a unique ability to colonize and persist in human and murine skin long term, resulting in nosocomial transmission and outbreaks of systemic infections.

    “Unlike other Candida species, such as Candida albicans, that colonize the intestine, C. auris has a unique ability to colonize and persist in human and murine skin long term, resulting in nosocomial transmission and outbreaks of systemic infections (4–8).”

    From Cell aggregation mediated by <i>ACE2</i> deletion in <i>Candida auris</i> modulates fungal colonization and host immune responses in the skin (2024) · cites this paper as [7]

    The Introduction’s “Persistent colonization of skin” section says C. auris can colonize people for months or up to a year, and “Clinical significance of persistent colonization” identifies skin colonization as the largest risk factor for later bloodstream infection. The Introduction also describes outbreaks in healthcare settings. Our copy does not establish long-term persistence on murine skin or an ability unique to C. auris among Candida species. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Unlike other Candida species, C. auris exhibits a distinct capacity for persistent skin colonization.

    “Unlike other Candida species, C. auris exhibits a distinct capacity for persistent skin colonization.”

    From Host–Candida auris interactions in the skin (2026) · cites this paper as [4]

    The Introduction’s “Persistent colonization of skin” section says C. auris can colonize patients’ skin for months or as long as a year. It also reports higher skin bioburden and denser ex vivo skin biofilms than other Candida species, but does not establish that persistent skin colonization itself distinguishes C. auris from other Candida species. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • C. auris exhibits a striking predilection for colonizing the human skin, enabling nosocomial transmission and outbreaks of fungemia and deep-seated infections.

    “C. auris exhibits a striking predilection for colonizing the human skin, enabling nosocomial transmission and outbreaks of fungemia and deep-seated infections [3–7].”

    From Host–Candida auris interactions in the skin (2026) · cites this paper as [4]

    The Introduction’s “Persistent colonization of skin” section identifies skin and nares as primary C. auris colonization sites and bloodstream infection as the major clinical risk. The Introduction also links long-term skin colonization to outbreaks in healthcare and other congregate settings. Our copy does not specifically describe outbreaks of deep-seated infections, so that part of the claim is not supported. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • C. auris has a unique ability to colonize and persist in human skin long term resulting in nosocomial transmission.

    “Unlike other Candida species such as Candida albicans that colonize the mammalian gastrointestinal tract, C. auris has a unique ability to colonize and persist in human skin long term resulting in nosocomial transmission (3–6).”

    From Yeast and filamentous <i>Candida auris</i> stimulate distinct immune responses in the skin (2024) · cites this paper as [5]

  • C. auris preferentially colonizes the human skin, leading to nosocomial transmission and outbreaks of systemic fungal infections.

    “Unlike other Candida species, such as Candida albicans that colonizes the intestinal tract, C. auris preferentially colonizes the human skin, leading to nosocomial transmission and outbreaks of systemic fungal infections [6–8].”

    From The Emerging Fungal Pathogen Candida auris Induces IFNγ to Colonize the Skin (2025) · cites this paper as [8]

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References 127 · Cited by 68

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  1. [1]Casadevall A, and Pirofski LA (2000). Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68, 6511– 6518. 10.1128/IAI.68.12.6511-6518.2000. 11083759 PMC97744 · DOI
  2. [2]Casadevall A, and Pirofski LA (2015). What is a host? Incorporating the microbiota into the damage-response framework. Infect Immun 83, 2– 7. 10.1128/IAI.02627-14. 25385796 PMC4288903 · DOI
  3. [5]Limon JJ, Skalski JH, and Underhill DM (2017). Commensal Fungi in Health and Disease. Cell Host Microbe 22, 156– 165. 10.1016/j.chom.2017.07.002. 28799901 PMC5573128 · DOI · Paper page
  4. [6]Rhimi W, Theelen B, Boekhout T, Otranto D, and Cafarchia C (2020). Malassezia spp. Yeasts of Emerging Concern in Fungemia. Front Cell Infect Microbiol 10, 370. 10.3389/fcimb.2020.00370. 32850475 PMC7399178 · DOI
  5. [7]Pedrosa AF, Lisboa C, and Rodrigues AG (2018). Malassezia infections with systemic involvement: Figures and facts. J Dermatol 45, 1278– 1282. 10.1111/1346-8138.14653. 30264900 · DOI
  6. [8]Vijaya Chandra SH, Srinivas R, Dawson TL Jr., and Common JE (2020). Cutaneous Malassezia: Commensal, Pathogen, or Protector? Front Cell Infect Microbiol 10, 614446. 10.3389/fcimb.2020.614446. 33575223 PMC7870721 · DOI
  7. [9]Rubin R (2022). On the Rise, Candida auris Outwits Treatments and Travels Incognito in Health Care Settings. JAMA. 10.1001/jama.2022.17760. 36576734 · DOI
  8. [10]Chow EWL, Pang LM, and Wang Y (2021). From Jekyll to Hyde: The Yeast-Hyphal Transition of Candida albicans. Pathogens 10. 10.3390/pathogens10070859. PMC8308684 34358008 · DOI
  9. [11]Witchley JN, Penumetcha P, Abon NV, Woolford CA, Mitchell AP, and Noble SM (2019). Candida albicans Morphogenesis Programs Control the Balance between Gut Commensalism and Invasive Infection. Cell Host Microbe 25, 432– 443 e436. 10.1016/j.chom.2019.02.008. 30870623 PMC6581065 · DOI
  10. [12]Pande K, Chen C, and Noble SM (2013). Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat Genet 45, 1088– 1091. 10.1038/ng.2710. 23892606 PMC3758371 · DOI · Paper page
  11. [13]Li XV, Leonardi I, Putzel GG, Semon A, Fiers WD, Kusakabe T, Lin WY, Gao IH, Doron I, Gutierrez-Guerrero A, (2022). Immune regulation by fungal strain diversity in inflammatory bowel disease. Nature 603, 672– 678. 10.1038/s41586-022-04502-w. 35296857 PMC9166917 · DOI
  12. [15]Chen H, He S, Zhang S, A R, Li W, and Liu S (2022). The Necrotroph Botrytis cinerea BcSpd1 Plays a Key Role in Modulating Both Fungal Pathogenic Factors and Plant Disease Development. Front Plant Sci 13, 820767. 10.3389/fpls.2022.820767. 35845699 PMC9280406 · DOI
  13. [16]Rolig AS, Sweeney EG, Kaye LE, DeSantis MD, Perkins A, Banse AV, Hamilton MK, and Guillemin K (2018). A bacterial immunomodulatory protein with lipocalin-like domains facilitates host-bacteria mutualism in larval zebrafish. Elife 7. 10.7554/eLife.37172. PMC6219842 30398151 · DOI
  14. [17]Jones DAB, John E, Rybak K, Phan HTT, Singh KB, Lin SY, Solomon PS, Oliver RP, and Tan KC (2019). A specific fungal transcription factor controls effector gene expression and orchestrates the establishment of the necrotrophic pathogen lifestyle on wheat. Sci Rep 9, 15884. 10.1038/s41598-019-52444-7. 31685928 PMC6828707 · DOI
  15. [18]Finkel-Jimenez B, Wuthrich M, and Klein BS (2002). BAD1, an essential virulence factor of Blastomyces dermatitidis, suppresses host TNF-alpha production through TGF-beta-dependent and -independent mechanisms. J Immunol 168, 5746– 5755. 10.4049/jimmunol.168.11.5746. 12023375 · DOI
  16. [19]Krappmann S, Bignell EM, Reichard U, Rogers T, Haynes K, and Braus GH (2004). The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol Microbiol 52, 785– 799. 10.1111/j.1365-2958.2004.04015.x. 15101984 · DOI · Paper page
  17. [20]Gao J, Chow EWL, Wang H, Xu X, Cai C, Song Y, Wang J, and Wang Y (2021). LncRNA DINOR is a virulence factor and global regulator of stress responses in Candida auris. Nat Microbiol 6, 842– 851. 10.1038/s41564-021-00915-x. 34083769 · DOI
  18. [21]Day AM, McNiff MM, da Silva Dantas A, Gow NAR, and Quinn J (2018). Hog1 Regulates Stress Tolerance and Virulence in the Emerging Fungal Pathogen Candida auris. mSphere 3. 10.1128/mSphere.00506-18. PMC6200985 30355673 · DOI · Paper page
  19. [22]Alanio A, Vernel-Pauillac F, Sturny-Leclere A, and Dromer F (2015). Cryptococcus neoformans host adaptation: toward biological evidence of dormancy. mBio 6. 10.1128/mBio.02580-14. PMC4453510 25827423 · DOI
  20. [24]Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV, and Knight R (2018). Current understanding of the human microbiome. Nat Med 24, 392– 400. 10.1038/nm.4517. 29634682 PMC7043356 · DOI · Paper page
  21. [25]Derrien M, and van Hylckama Vlieg JE (2015). Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol 23, 354– 366. 10.1016/j.tim.2015.03.002. 25840765 · DOI · Paper page
  22. [27]Runge S, and Rosshart SP (2021). The Mammalian Metaorganism: A Holistic View on How Microbes of All Kingdoms and Niches Shape Local and Systemic Immunity. Front Immunol 12, 702378. 10.3389/fimmu.2021.702378. 34276696 PMC8278200 · DOI
  23. [28]Relman DA (2012). The human microbiome: ecosystem resilience and health. Nutr Rev 70 Suppl 1, S2– 9. 10.1111/j.1753-4887.2012.00489.x. 22861804 PMC3422777 · DOI
  24. [29]Jo JH, Harkins CP, Schwardt NH, Portillo JA, Program NCS, Zimmerman MD, Carter CL, Hossen MA, Peer CJ, Polley EC, (2021). Alterations of human skin microbiome and expansion of antimicrobial resistance after systemic antibiotics. Sci Transl Med 13, eabd8077. 10.1126/scitranslmed.abd8077. 34936382 PMC8878148 · DOI
  25. [30]Pankhurst CL (2013). Candidiasis (oropharyngeal). BMJ Clin Evid 2013, 1304. PMC3821534 24209593
  26. [31]Goncalves B, Ferreira C, Alves CT, Henriques M, Azeredo J, and Silva S (2016). Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol 42, 905– 927. 10.3109/1040841X.2015.1091805. 26690853 · DOI · Paper page
  27. [32]Seelbinder B, Chen J, Brunke S, Vazquez-Uribe R, Santhaman R, Meyer AC, de Oliveira Lino FS, Chan KF, Loos D, Imamovic L, (2020). Antibiotics create a shift from mutualism to competition in human gut communities with a longer-lasting impact on fungi than bacteria. Microbiome 8, 133. 10.1186/s40168-020-00899-6. 32919472 PMC7488854 · DOI
  28. [33]Zhai B, Ola M, Rolling T, Tosini NL, Joshowitz S, Littmann ER, Amoretti LA, Fontana E, Wright RJ, Miranda E, (2020). High-resolution mycobiota analysis reveals dynamic intestinal translocation preceding invasive candidiasis. Nat Med 26, 59– 64. 10.1038/s41591-019-0709-7. 31907459 PMC7005909 · DOI
  29. [34]Wheeler ML, Limon JJ, Bar AS, Leal CA, Gargus M, Tang J, Brown J, Funari VA, Wang HL, Crother TR, (2016). Immunological Consequences of Intestinal Fungal Dysbiosis. Cell Host Microbe 19, 865– 873. 10.1016/j.chom.2016.05.003. 27237365 PMC4900921 · DOI
  30. [35]O’Horo JC, Silva GL, Munoz-Price LS, and Safdar N (2012). The efficacy of daily bathing with chlorhexidine for reducing healthcare-associated bloodstream infections: a meta-analysis. Infect Control Hosp Epidemiol 33, 257– 267. 10.1086/664496. 22314063 · DOI
  31. [36]SanMiguel AJ, Meisel JS, Horwinski J, Zheng Q, Bradley CW, and Grice EA (2018). Antiseptic Agents Elicit Short-Term, Personalized, and Body Site-Specific Shifts in Resident Skin Bacterial Communities. J Invest Dermatol 138, 2234– 2243. 10.1016/j.jid.2018.04.022. 29753031 PMC6326167 · DOI · Paper page
  32. [38]Afeltra J, and Verweij PE (2003). Antifungal Activity of Nonantifungal Drugs. European Journal of Clinical Microbiology and Infectious Diseases 22, 397– 407. 10.1007/s10096-003-0947-x. 12884072 · DOI · Paper page
  33. [39]Proctor DM, and Relman DA (2017). The Landscape Ecology and Microbiota of the Human Nose, Mouth, and Throat. Cell Host Microbe 21, 421– 432. 10.1016/j.chom.2017.03.011. 28407480 PMC5538306 · DOI
  34. [40]Dawes C (1972). Circadian rhythms in human salivary flow rate and composition. J Physiol 220, 529– 545. 10.1113/jphysiol.1972.sp009721. 5016036 PMC1331668 · DOI
  35. [41]Collado MC, Engen PA, Bandin C, Cabrera-Rubio R, Voigt RM, Green SJ, Naqib A, Keshavarzian A, Scheer F, and Garaulet M (2018). Timing of food intake impacts daily rhythms of human salivary microbiota: a randomized, crossover study. FASEB J 32, 2060– 2072. 10.1096/fj.201700697RR. 29233857 PMC5893176 · DOI · Paper page
  36. [42]Prado-Mel E, Ciudad-Gutierrez P, Rodriguez-Ramallo H, Sanchez-Fidalgo S, Santos-Ramos B, and Villalba-Moreno AM (2022). Association between anticholinergic activity and xerostomia and/ or xerophthalmia in the elderly: systematic review. BMC Pharmacol Toxicol 23, 94. 10.1186/s40360-022-00637-8. 36539885 PMC9769019 · DOI
  37. [43]Dreizen S, Brown LR, Handler S, and Levy BM (1976). Radiation-induced xerostomia in cancer patients. Effect on salivary and serum electrolytes. Cancer 38, 273– 278. 7352
  38. [45]Ooshima T, Hashida T, Fuchihata H, Fujiwara T, Yoshida T, Izumitani A, Sobue S, and Hamada S (1991). Dental caries induction in hyposalivated rats. Caries Res 25, 138– 142. 10.1159/000261356. 2059975 · DOI
  39. [46]Molek M, Florenly F, Lister INE, Wahab TA, Lister C, and Fioni F (2022). Xerostomia and hyposalivation in association with oral candidiasis: a systematic review and meta-analysis. Evid Based Dent. 10.1038/s41432-021-0210-2. 35075251 · DOI
  40. [47]Park J, Schwardt NH, Jo JH, Zhang Z, Pillai V, Phang S, Brady SM, Portillo JA, MacGibeny MA, Liang H, (2022). Shifts in the Skin Bacterial and Fungal Communities of Healthy Children Transitioning through Puberty. J Invest Dermatol 142, 212– 219. 10.1016/j.jid.2021.04.034. 34252398 PMC8688298 · DOI
  41. [48]Russell-Goldman E, and Murphy GF (2020). The Pathobiology of Skin Aging: New Insights into an Old Dilemma. Am J Pathol 190, 1356– 1369. 10.1016/j.ajpath.2020.03.007. 32246919 PMC7481755 · DOI
  42. [49]O’Loughlin LS, and Green PT (2017). Secondary invasion: When invasion success is contingent on other invaders altering the properties of recipient ecosystems. Ecol Evol 7, 7628– 7637. 10.1002/ece3.3315. 29043020 PMC5632608 · DOI
  43. [50]Pang IK, and Iwasaki A (2012). Control of antiviral immunity by pattern recognition and the microbiome. Immunol Rev 245, 209– 226. 10.1111/j.1600-065X.2011.01073.x. 22168422 PMC3659816 · DOI
  44. [52]Kurkjian HM, Akbari MJ, and Momeni B (2021). The impact of interactions on invasion and colonization resistance in microbial communities. PLoS Comput Biol 17, e1008643. 10.1371/journal.pcbi.1008643. 33481772 PMC7857599 · DOI
  45. [53]Rao C, Coyte KZ, Bainter W, Geha RS, Martin CR, and Rakoff-Nahoum S (2021). Multi-kingdom ecological drivers of microbiota assembly in preterm infants. Nature 591, 633– 638. 10.1038/s41586-021-03241-8. 33627867 PMC7990694 · DOI
  46. [55]Larson PJ, Zhou W, Santiago A, Driscoll S, Fleming E, Voigt AY, Chun OK, Grady JJ, Kuchel GA, Robison JT, and Oh J (2022). Associations of the skin, oral and gut microbiome with aging, frailty and infection risk reservoirs in older adults. Nat Aging 2, 941– 955. 10.1038/s43587-022-00287-9. 36398033 PMC9667708 · DOI
  47. [56]Pappas PG, Lionakis MS, Arendrup MC, Ostrosky-Zeichner L, and Kullberg BJ (2018). Invasive candidiasis. Nature Reviews Disease Primers 4, 18026. 10.1038/nrdp.2018.26. 29749387 · DOI · Paper page
  48. [58]Mishra AA, and Koh AY (2018). Adaptation of Candida albicans during gastrointestinal tract colonization. Curr Clin Microbiol Rep 5, 165– 172. 10.1007/s40588-018-0096-8. 30560045 PMC6294318 · DOI
  49. [59]Heisel T, Montassier E, Johnson A, Al-Ghalith G, Lin YW, Wei LN, Knights D, and Gale CA (2017). High-Fat Diet Changes Fungal Microbiomes and Interkingdom Relationships in the Murine Gut. mSphere 2. 10.1128/mSphere.00351-17. PMC5636226 29034327 · DOI
  50. [61]Dohlman AB, Klug J, Mesko M, Gao IH, Lipkin SM, Shen X, and Iliev ID (2022). A pan-cancer mycobiome analysis reveals fungal involvement in gastrointestinal and lung tumors. Cell 185, 3807– 3822 e3812. 10.1016/j.cell.2022.09.015. 36179671 PMC9564002 · DOI
  51. [62]Bacher P, Jochheim-Richter A, Mockel-Tenbrink N, Kniemeyer O, Wingenfeld E, Alex R, Ortigao A, Karpova D, Lehrnbecher T, Ullmann AJ, (2015). Clinical-scale isolation of the total Aspergillus fumigatus-reactive T-helper cell repertoire for adoptive transfer. Cytotherapy 17, 1396– 1405. 10.1016/j.jcyt.2015.05.011. 26188965 · DOI
  52. [63]Yang AM, Inamine T, Hochrath K, Chen P, Wang L, Llorente C, Bluemel S, Hartmann P, Xu J, Koyama Y, (2017). Intestinal fungi contribute to development of alcoholic liver disease. J Clin Invest 127, 2829– 2841. 10.1172/JCI90562. 28530644 PMC5490775 · DOI
  53. [65]McDonough LD, Mishra AA, Tosini N, Kakade P, Penumutchu S, Liang SH, Maufrais C, Zhai B, Taur Y, Belenky P, (2021). Candida albicans Isolates 529L and CHN1 Exhibit Stable Colonization of the Murine Gastrointestinal Tract. mBio 12, e0287821. 10.1128/mBio.02878-21. 34724818 PMC8561340 · DOI
  54. [68]Liang SH, Anderson MZ, Hirakawa MP, Wang JM, Frazer C, Alaalm LM, Thomson GJ, Ene IV, and Bennett RJ (2019). Hemizygosity Enables a Mutational Transition Governing Fungal Virulence and Commensalism. Cell Host Microbe 25, 418– 431 e416. 10.1016/j.chom.2019.01.005. 30824263 PMC6624852 · DOI
  55. [72]Drummond RA, Desai JV, Ricotta EE, Swamydas M, Deming C, Conlan S, Quinones M, Matei-Rascu V, Sherif L, Lecky D, (2022). Long-term antibiotic exposure promotes mortality after systemic fungal infection by driving lymphocyte dysfunction and systemic escape of commensal bacteria. Cell Host Microbe. 10.1016/j.chom.2022.04.013. PMC9283303 35568028 · DOI · Paper page
  56. [73]Basso P, Dang EV, Urisman A, Cowen LE, Madhani HD, and Noble SM (2022). Deep tissue infection by an invasive human fungal pathogen requires lipid-based suppression of the IL-17 response. Cell Host Microbe 30, 1589– 1601.e1585. 10.1016/j.chom.2022.10.004. 36323314 PMC9744107 · DOI
  57. [74]Shao T-Y, Ang WXG, Jiang TT, Huang FS, Andersen H, Kinder JM, Pham G, Burg AR, Ruff B, Gonzalez T, (2019). Commensal Candida albicans Positively Calibrates Systemic Th17 Immunological Responses. Cell Host Microbe 25, 404– 417.e406. 10.1016/j.chom.2019.02.004. 30870622 PMC6419754 · DOI
  58. [75]Tso GHW, Reales-Calderon JA, Tan ASM, Sem X, Le GTT, Tan TG, Lai GC, Srinivasan KG, Yurieva M, Liao W, (2018). Experimental evolution of a fungal pathogen into a gut symbiont. Science 362, 589– 595. 10.1126/science.aat0537. 30385579 · DOI
  59. [76]Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, Panzer AR, LaMere B, Rackaityte E, Lukacs NW, (2016). Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nature Medicine 22, 1187– 1191. 10.1038/nm.4176. PMC5053876 27618652 · DOI
  60. [77]Wu Y, Zeng Z, Guo Y, Song L, Weatherhead JE, Huang X, Zeng Y, Bimler L, Chang CY, Knight JM, (2021). Candida albicans elicits protective allergic responses via platelet mediated T helper 2 and T helper 17 cell polarization. Immunity 54, 2595– 2610 e2597. 10.1016/j.immuni.2021.08.009. 34506733 PMC8585696 · DOI
  61. [78]Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, Höfs S, Gratacap RL, Robbins J, Runglall M, (2016). Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 532, 64– 68. 10.1038/nature17625. 27027296 PMC4851236 · DOI
  62. [79]Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, Colombo AL, Calvo B, Cuomo CA, Desjardins CA, (2017). Simultaneous Emergence of Multidrug-Resistant Candida auris on 3 Continents Confirmed by Whole-Genome Sequencing and Epidemiological Analyses. Clin Infect Dis 64, 134– 140. 10.1093/cid/ciw691. 27988485 PMC5215215 · DOI · Paper page
  63. [80]Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, and Jang HC (2011). First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol 49, 3139– 3142. 10.1128/JCM.00319-11. 21715586 PMC3165631 · DOI
  64. [82]Thoma R, Seneghini M, Seiffert SN, Vuichard Gysin D, Scanferla G, Haller S, Flury D, Boggian K, Kleger GR, Filipovic M, (2022). The challenge of preventing and containing outbreaks of multidrug-resistant organisms and Candida auris during the coronavirus disease 2019 pandemic: report of a carbapenem-resistant Acinetobacter baumannii outbreak and a systematic review of the literature. Antimicrob Resist Infect Control 11, 12. 10.1186/s13756-022-01052-8. 35063032 PMC8777447 · DOI
  65. [83]CDC. Antibiotic Resistance Threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019. 10.15620/cdc:82532. · DOI · Paper page
  66. [84]Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, Kemble SK, Pacilli M, Black SR, Landon E, (2016). Investigation of the First Seven Reported Cases of Candida auris, a Globally Emerging Invasive, Multidrug-Resistant Fungus - United States, May 2013-August 2016. MMWR Morb Mortal Wkly Rep 65, 1234– 1237. 10.15585/mmwr.mm6544e1. 27832049 · DOI · Paper page
  67. [85]Zhu Y, O’Brien B, Leach L, Clarke A, Bates M, Adams E, Ostrowsky B, Quinn M, Dufort E, Southwick K, (2020). Laboratory Analysis of an Outbreak of Candida auris in New York from 2016 to 2018: Impact and Lessons Learned. J Clin Microbiol 58. 10.1128/JCM.01503-19. PMC7098748 31852764 · DOI
  68. [87]Ghannoum M, Herrada J, McCormick TS, and Long L (2021). A Novel Transdermal Application for Clearing Skin Colonization by Candida auris. Antimicrobial Agents and Chemotherapy 65, e02303– 02320. doi: 10.1128/AAC.02303-20. PMC8092864 33558297 · DOI
  69. [88]Huang X, Hurabielle C, Drummond RA, Bouladoux N, Desai JV, Sim CK, Belkaid Y, Lionakis MS, and Segre JA (2021). Murine model of colonization with fungal pathogen Candida auris to explore skin tropism, host risk factors and therapeutic strategies. Cell Host Microbe 29, 210– 221 e216. 10.1016/j.chom.2020.12.002. 33385336 PMC7878403 · DOI · Paper page
  70. [89]Borman AM, Szekely A, and Johnson EM (2016). Comparative Pathogenicity of United Kingdom Isolates of the Emerging Pathogen Candida auris and Other Key Pathogenic Candida Species. mSphere 1. 10.1128/mSphere.00189-16. PMC4990711 27547827 · DOI · Paper page
  71. [91]Schelenz S, Hagen F, Rhodes JL, Abdolrasouli A, Chowdhary A, Hall A, Ryan L, Shackleton J, Trimlett R, Meis JF, (2016). First hospital outbreak of the globally emerging Candida auris in a European hospital. Antimicrobial Resistance & Infection Control 5, 35. 10.1186/s13756-016-0132-5. 27777756 PMC5069812 · DOI · Paper page
  72. [92]Eyre DW, Sheppard AE, Madder H, Moir I, Moroney R, Quan TP, Griffiths D, George S, Butcher L, Morgan M, (2018). A Candida auris Outbreak and Its Control in an Intensive Care Setting. N Engl J Med 379, 1322– 1331. 10.1056/NEJMoa1714373. 30281988 · DOI · Paper page
  73. [93]Roberts SC, Zembower TR, Ozer EA, and Qi C (2021). Genetic Evaluation of Nosocomial Candida auris Transmission. J Clin Microbiol 59. 10.1128/JCM.02252-20. PMC8092739 33472901 · DOI
  74. [94]de St Maurice A, Parti U, Anikst VE, Harper T, Mirasol R, Dayo AJ, Garner OB, Prabaker KK, and Yang S (2022). Clinical, microbiological, and genomic characteristics of clade-III Candida auris colonization and infection in southern California, 2019-2022. Infect Control Hosp Epidemiol, 1– 9. 10.1017/ice.2022.204. PMC10369217 36052507 · DOI
  75. [95]De Luca DG, Alexander DC, Dingle TC, Dufresne PJ, Hoang LM, Kus JV, Schwartz IS, Mulvey MR, and Bharat A (2022). Four genomic clades of Candida auris identified in Canada, 2012-2019. Med Mycol 60. 10.1093/mmy/myab079. 34910140 · DOI · Paper page
  76. [96]Yadav A, Jain K, Wang Y, Pawar K, Kaur H, Sharma KK, Tripathy V, Singh A, Xu J, and Chowdhary A (2022). Candida auris on Apples: Diversity and Clinical Significance. mBio 13, e0051822. 10.1128/mbio.00518-22. 35357170 PMC9040835 · DOI
  77. [97]Markussen T, Marvig RL, Gomez-Lozano M, Aanaes K, Burleigh AE, Hoiby N, Johansen HK, Molin S, and Jelsbak L (2014). Environmental heterogeneity drives within-host diversification and evolution of Pseudomonas aeruginosa. mBio 5, e01592– 01514. 10.1128/mBio.01592-14. 25227464 PMC4172072 · DOI
  78. [98]Bartell JA, Sommer LM, Haagensen JAJ, Loch A, Espinosa R, Molin S, and Johansen HK (2019). Evolutionary highways to persistent bacterial infection. Nat Commun 10, 629. 10.1038/s41467-019-08504-7. 30733448 PMC6367392 · DOI
  79. [99]Lieberman TD, Flett KB, Yelin I, Martin TR, McAdam AJ, Priebe GP, and Kishony R (2014). Genetic variation of a bacterial pathogen within individuals with cystic fibrosis provides a record of selective pressures. Nat Genet 46, 82– 87. 10.1038/ng.2848. 24316980 PMC3979468 · DOI
  80. [100]Burrack LS, Todd RT, Soisangwan N, Wiederhold NP, and Selmecki A (2022). Genomic Diversity across Candida auris Clinical Isolates Shapes Rapid Development of Antifungal Resistance In Vitro and In Vivo. mBio 13, e0084222. 10.1128/mbio.00842-22. 35862787 PMC9426540 · DOI · Paper page
  81. [101]Gambhir N, Harris SD, and Everhart SE (2022). Evolutionary Significance of Fungal Hypermutators: Lessons Learned from Clinical Strains and Implications for Fungal Plant Pathogens. mSphere 7, e0008722. 10.1128/msphere.00087-22. 35638358 PMC9241500 · DOI
  82. [103]Forche A, Cromie G, Gerstein AC, Solis NV, Pisithkul T, Srifa W, Jeffery E, Abbey D, Filler SG, Dudley AM, and Berman J (2018). Rapid Phenotypic and Genotypic Diversification After Exposure to the Oral Host Niche in Candida albicans. Genetics 209, 725– 741. 10.1534/genetics.118.301019. 29724862 PMC6028260 · DOI · Paper page
  83. [104]Helmstetter N, Chybowska AD, Delaney C, Da Silva Dantas A, Gifford H, Wacker T, Munro C, Warris A, Jones B, Cuomo CA, (2022). Population genetics and microevolution of clinical Candida glabrata reveals recombinant sequence types and hypervariation within mitochondrial genomes, virulence genes, and drug targets. Genetics 221. 10.1093/genetics/iyac031. PMC9071574 35199143 · DOI
  84. [106]Calvo B, Melo AS, Perozo-Mena A, Hernandez M, Francisco EC, Hagen F, Meis JF, and Colombo AL (2016). First report of Candida auris in America: Clinical and microbiological aspects of 18 episodes of candidemia. J Infect 73, 369– 374. 10.1016/j.jinf.2016.07.008. 27452195 · DOI
  85. [107]Ben-Ami R, Olshtain-Pops K, Krieger M, Oren I, Bishara J, Dan M, Wiener-Well Y, Weinberger M, Zimhony O, Chowers M, (2012). Antibiotic exposure as a risk factor for fluconazole-resistant Candida bloodstream infection. Antimicrob Agents Chemother 56, 2518– 2523. 10.1128/AAC.05947-11. 22314534 PMC3346668 · DOI
  86. [108]Huang X, Welsh RM, Deming C, Proctor DM, Thomas PJ, Gussin GM, Huang SS, Kong HH, Bentz ML, Vallabhaneni S, (2021). Skin Metagenomic Sequence Analysis of Early Candida auris Outbreaks in U.S. Nursing Homes. mSphere 6, e00287– 00221. doi: 10.1128/mSphere.00287-21. 34346704 PMC8386442 · DOI
  87. [109]Pichowicz AM, Torres SR, Torres-Velez FJ, Longyear AD, Singh N, Lasek-Nesselquist E, and De Jesus M (2022). Depletion of the Microbiota Has a Modest but Important Impact on the Fungal Burden of the Heart and Lungs during Early Systemic Candida auris Infection in Neutropenic Mice. Microorganisms 10. 10.3390/microorganisms10020330. PMC8874628 35208785 · DOI
  88. [110]Huang D, Li H, Lin Y, Lin J, Li C, Kuang Y, Zhou W, Huang B, and Wang P (2022). Antibiotic-induced depletion of Clostridium species increases the risk of secondary fungal infections in preterm infants. Front Cell Infect Microbiol 12, 981823. 10.3389/fcimb.2022.981823. 36118040 PMC9473543 · DOI
  89. [113]Jiang TT, Shao TY, Ang WXG, Kinder JM, Turner LH, Pham G, Whitt J, Alenghat T, and Way SS (2017). Commensal Fungi Recapitulate the Protective Benefits of Intestinal Bacteria. Cell Host Microbe 22, 809– 816 e804. 10.1016/j.chom.2017.10.013. 29174402 PMC5730478 · DOI
  90. [114]Shirtliff ME, Peters BM, and Jabra-Rizk MA (2009). Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299, 1– 8. 10.1111/j.1574-6968.2009.01668.x. 19552706 PMC4406406 · DOI
  91. [115]Sayeed MA, Farooqi J, Jabeen K, Awan S, and Mahmood SF (2019). Clinical spectrum and factors impacting outcome of Candida auris: a single center study from Pakistan. BMC Infect Dis 19, 384. 10.1186/s12879-019-3999-y. 31060514 PMC6501321 · DOI
  92. [116]Tian S, Bing J, Chu Y, Chen J, Cheng S, Wang Q, Zhang J, Ma X, Zhou B, Liu L, (2021). Genomic epidemiology of Candida auris in a general hospital in Shenyang, China: a three-year surveillance study. Emerg Microbes Infect 10, 1088– 1096. 10.1080/22221751.2021.1934557. 34027824 PMC8183536 · DOI
  93. [117]Boomer JS, Green JM, and Hotchkiss RS (2014). The changing immune system in sepsis: is individualized immuno-modulatory therapy the answer? Virulence 5, 45– 56. 10.4161/viru.26516. 24067565 PMC3916383 · DOI
  94. [118]Venet F, and Monneret G (2018). Advances in the understanding and treatment of sepsis-induced immunosuppression. Nat Rev Nephrol 14, 121– 137. 10.1038/nrneph.2017.165. 29225343 · DOI
  95. [119]Otto GP, Sossdorf M, Claus RA, Rodel J, Menge K, Reinhart K, Bauer M, and Riedemann NC (2011). The late phase of sepsis is characterized by an increased microbiological burden and death rate. Crit Care 15, R183. 10.1186/cc10332. 21798063 PMC3387626 · DOI
  96. [120]Pittet D, Li N, and Wenzel RP (1993). Association of secondary and polymicrobial nosocomial bloodstream infections with higher mortality. Eur J Clin Microbiol Infect Dis 12, 813– 819. 10.1007/BF02000400. 8112351 · DOI
  97. [121]Gleckman R, Blagg N, and Joubert DW (1981). Trimethoprim: mechanisms of action, antimicrobial activity, bacterial resistance, pharmacokinetics, adverse reactions, and therapeutic indications. Pharmacotherapy 1, 14– 20. 10.1002/j.1875-9114.1981.tb03548.x. 6985448 · DOI
  98. [122]Stevens DA, and Vo PT (1982). Synergistic interaction of trimethoprim and sulfamethoxazole on Paracoccidioides brasiliensis. Antimicrobial Agents and Chemotherapy 21, 852– 854. doi: 10.1128/AAC.21.5.852. 7103462 PMC182028 · DOI
  99. [123]Afeltra J, Meis JFGM, Vitale RG, Mouton JW, and Verweij PE (2002). In Vitro Activities of Pentamidine, Pyrimethamine, Trimethoprim, and Sulfonamides against Aspergillus Species. Antimicrobial Agents and Chemotherapy 46, 2029– 2031. doi: 10.1128/AAC.46.6.2029-2031.2002. 12019133 PMC127271 · DOI
  100. [124]Lionakis MS, Chamilos G, Lewis RE, Wiederhold NP, Raad II, Samonis G, and Kontoyiannis DP (2006). Pentamidine is active in a neutropenic murine model of acute invasive pulmonary fusariosis. Antimicrob Agents Chemother 50, 294– 297. 10.1128/AAC.50.1.294-297.2006. 16377700 PMC1346817 · DOI
  101. [125]Lionakis MS, Lewis RE, Samonis G, and Kontoyiannis DP (2003). Pentamidine is active in vitro against Fusarium species. Antimicrob Agents Chemother 47, 3252– 3259. 10.1128/AAC.47.10.3252-3259.2003. 14506038 PMC201137 · DOI
  102. [126]Foley GE, and Winter WD Jr. (1949). Increased mortality following penicillin therapy of chick embryos infected with Candida albicans var. stellatoidea. J Infect Dis 85, 268– 274. 10.1093/infdis/85.3.268. 15406848 · DOI
  103. [127]Huppert M, Macpherson DA, and Cazin J (1953). Pathogenesis of Candida albicans infection following antibiotic therapy. I. The effect of antibiotics on the growth of Candida albicans. J Bacteriol 65, 171– 176. 10.1128/jb.65.2.171-176.1953. 13034711 PMC169661 · DOI
  104. [128]Maione A, Pietra AL, Salvatore MM, Guida M, Galdiero E, and de Alteriis E (2022). Undesired Effect of Vancomycin Prolonged Treatment: Enhanced Biofilm Production of the Nosocomial Pathogen Candida auris. Antibiotics 11, 1771. 36551428 PMC9774269
  105. [129]Melenotte C, Pontarotti P, Pinault L, Mege JL, Devaux C, and Raoult D (2021). Could beta-Lactam Antibiotics Block Humoral Immunity? Front Immunol 12, 680146. 10.3389/fimmu.2021.680146. 34603278 PMC8480522 · DOI

Authors
Proctor, D. M., Drummond, R. A., Lionakis, M. S., & Segre, J. A.
Affiliations
  • National Institutes of Health (US)
  • University of Birmingham (GB)
Corresponding author
Proctor, Diana M.
ORCID
Venue
Cell Host & Microbe
Publisher
Elsevier BV
Published
2023-04
Volume
31
Issue
4
Pages
539-553
ISSN
1931-3128 (ISSN-L)
DOI
10.1016/j.chom.2023.02.010
PMC
PMC10155287
OpenAlex
W4365137016
Cited by
68
References
127
Citations by year
2026: 14 · 2025: 20 · 2024: 26 · 2023: 8
FWCI
3.22
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell Host & Microbe (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-sa)
  • Digital Commons-TMC (Texas Medical Center) (submittedVersion)
Funders
  • National Institute of Allergy and Infectious Diseases
  • Canadian Institute for Advanced Research
  • National Institutes of Health
  • National Human Genome Research Institute
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords
Candida auris, Candida albicans, commensalism, pathogenesis, invasive candidiasis, fungal colonization, host immunity, antibiotic exposure, host-fungus interactions
MeSH terms
Mycobiome, Candida albicans, Candidiasis, Humans, Symbiosis, Host-Pathogen Interactions, Candidiasis, Invasive

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