Infant fungal communities: Current knowledge and research opportunities

BMC Medicine

Volumn 15, Issue 1, 2017, Pages

  Ward, Tonya L ^a   Knights, Dan ^a,b   Gale, Cheryl A ^c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Bacteria; Development; Fungi; Infant; Microbiome; Microbiota; Mycobiome; Mycobiota

Indexed keywords

ALLERGIC DISEASE; ANTIBIOTIC THERAPY; BACTERIUM; BACTERIUM FUNGUS INTERACTION; DATA BASE; DIARRHEA; DIET; ENVIRONMENTAL FACTOR; FUNGAL COMMUNITY; GENETICS; GESTATIONAL AGE; HEALTH; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; LONGITUDINAL STUDY; MONITORING; MOTHER; MYCOBIOME; NONHUMAN; OBESITY; OBSTETRIC DELIVERY; ORGANISMAL INTERACTION; OUTCOME ASSESSMENT; QUANTITATIVE ANALYSIS; REVIEW; FUNGUS; MICROFLORA; PATHOGENICITY;

FUNGI; HUMANS; MICROBIOTA;

EID: 85012124697     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/s12916-017-0802-z     Document Type: Review

References (93)

1. Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med. 2016;22:713-22.
2. Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD, et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One. 2013;8, e66019.
3. Rajilić-Stojanović M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. Fems Microbiol Rev. 2014;38:996-1047.
4. Balan P, B Gogineni S, Kumari NS, Shetty V, Lakshman Rangare A, L Castelino R, et al. Candida carriage rate and growth characteristics of saliva in diabetes mellitus patients: A case-control study. J Dent Res Dent Clin Dent Prospects. 2015;9:274-9.
5. Giraldo P, von Nowaskonski A, Gomes FA, Linhares I, Neves NA, Witkin SS. Vaginal colonization by Candida in asymptomatic women with and without a history of recurrent vulvovaginal candidiasis. Obstet Gynecol. 2000;95:413-6.
6. Moré MI, Swidsinski A. Saccharomyces boulardii CNCM I-745 supports regeneration of the intestinal microbiota after diarrheic dysbiosis - a review. Clin Exp Gastroenterol. 2015;8:237-55.
7. Zanello G, Meurens F, Berri M, Salmon H. Saccharomyces boulardii effects on gastrointestinal diseases. Curr Issues Mol Biol. 2009;11:47-58.
8. Coates EW, Karlowicz MG, Croitoru DP, Buescher ES. Distinctive distribution of pathogens associated with peritonitis in neonates with focal intestinal perforation compared with necrotizing enterocolitis. Pediatrics. 2005;116:e241-6.
9. Ragouilliaux CJ, Keeney SE, Hawkins HK, Rowen JL. Maternal factors in extremely low birth weight infants who develop spontaneous intestinal perforation. Pediatrics. 2007;120:e1458-64.
10. Saiman L, Ludington E, Pfaller M, Rangel-Frausto S, Wiblin RT, Dawson J, et al. Risk factors for candidemia in Neonatal Intensive Care Unit patients. Pediatr Infect Dis J. 2000;19:319-24.
11. Suhr MJ, Hallen-Adams HE. The human gut mycobiome: pitfalls and potentials--a mycologist's perspective. Mycologia. 2015;107:1057-73.
12. Underhill DM, Iliev ID. The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol. 2014;14:405-16.
13. Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson K-H, Kõljalg U. Taxonomic reliability of DNA sequences in public sequence databases: A fungal perspective. PLoS One. 2006;1, e59.
14. Heisel T, Podgorski H, Staley CM, Knights D, Sadowsky MJ, Gale CA. Complementary amplicon-based genomic approaches for the study of fungal communities in humans. PLoS One. 2015;10, e0116705.
15. Lim ES, Wang D, Holtz LR. The bacterial microbiome and virome milestones of infant development. Trends Microbiol. 2016;24(10):801-10.
16. Vangay P, Ward T, Gerber JS, Knights D. Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe. 2015;17:553-64.
17. Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109-17.
18. Martin R, Makino H, Yavuz AC, Ben-Amor K, Roelofs M, Ishikawa E, et al. Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS One. 2016;11, e0158498.
19. Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review. BMC Gastroenterol. 2016;16:86.
20. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690-703.
21. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971-5.
22. Bliss JM, Basavegowda KP, Watson WJ, Sheikh AU, Ryan RM. Vertical and horizontal transmission of Candida albicans in very low birth weight infants using DNA fingerprinting techniques. Pediatr Infect Dis J. 2008;27:231-5.
23. Soll DR, Galask R, Schmid J, Hanna C, Mac K, Morrow B. Genetic dissimilarity of commensal strains of Candida spp. carried in different anatomical locations of the same healthy women. J Clin Microbiol. 1991;29:1702-10.
24. Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspõllu A, Väin E, et al. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One. 2013;8, e54379.
25. Pandey PK, Siddharth J, Verma P, Bavdekar A, Patole MS, Shouche YS. Molecular typing of fecal eukaryotic microbiota of human infants and their respective mothers. J Biosci. 2012;37:221-6.
26. LaTuga MS, Ellis JC, Cotton CM, Goldberg RN, Wynn JL, Jackson RB, et al. Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants. PLoS One. 2011;6, e27858.
27. Strati F, Di Paola M, Stefanini I, Albanese D, Rizzetto L, Lionetti P, et al. Age and gender affect the composition of fungal population of the human gastrointestinal tract. Front Microbiol. 2016;7:1227.
28. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5, e177.
29. Mar Rodríguez M, Pérez D, Javier Chaves F, Esteve E, Marin-Garcia P, Xifra G, et al. Obesity changes the human gut mycobiome. Sci Rep. 2015;5:14600.
30. Chen Y, Chen Z, Guo R, Chen N, Lu H, Huang S, et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn Microbiol Infect Dis. 2011;70:492-8.
31. Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J, et al. Altered gut microbiota in Rett syndrome. Microbiome. 2016;4:41.
32. Ott SJ, Kühbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol. 2008;43:831-41.
33. Hallen-Adams HE, Kachman SD, Kim J, Legge RM, Martínez I. Fungi inhabiting the healthy human gastrointestinal tract: a diverse and dynamic community. Fungal Ecol. 2015;15:9-17.
34. Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, et al. Topographic diversity of fungal and bacterial communities in human skin. Nature. 2013;498:367-70.
35. Nagata R, Nagano H, Ogishima D, Nakamura Y, Hiruma M, Sugita T. Transmission of the major skin microbiota, Malassezia, from mother to neonate. Pediatr Int. 2012;54:350-5.
36. Park HK, Ha M-H, Park S-G, Kim MN, Kim BJ, Kim W. Characterization of the fungal microbiota (mycobiome) in healthy and dandruff-afflicted human scalps. PLoS One. 2012;7, e32847.
37. Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T. Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol. 2011;55:625-32.
38. Paulino LC, Tseng C-H, Blaser MJ. Analysis of Malassezia microbiota in healthy superficial human skin and in psoriatic lesions by multiplex real-time PCR. FEMS Yeast Res. 2008;8:460-71.
39. Paulino LC, Tseng C-H, Strober BE, Blaser MJ. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clin Microbiol. 2006;44:2933-41.
40. Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H. ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol. 2010;10:189.
41. Koenig JE, Fricker AD, Scalfon N, Kotman N, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A. 2011;108:4578-85.
42. Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2014;16:2891-904.
43. Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96:544-51.
44. Hunt KM, Foster JA, Forney LJ, Schütte UME, Beck DL, Abdo Z, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One. 2011;6, e21313.
45. De Leoz MLA, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, et al. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. J Proteome Res. 2015;14:491-502.
46. Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, et al. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem. 2011;286:34583-92.
47. Mutschlechner W, Karall D, Hartmann C, Streiter B, Baumgartner-Sigl S, Orth-Höller D, et al. Mammary candidiasis: molecular-based detection of Candida species in human milk samples. Eur J Clin Microbiol Infect Dis. 2016;35:1309-13.
48. Gonia S, Tuepker M, Heisel T, Autran C, Bode L, Gale CA. Human milk oligosaccharides inhibit Candida albicans invasion of human premature intestinal epithelial cells. J Nutr. 2015;145:1992-8.
49. Holgerson PL, Vestman NR, Claesson R, Öhman C, Domellöf M, Tanner AC, et al. Oral microbial profile discriminates breastfed from formula-fed Infants. J Pediatr Gastroenterol Nutr. 2013;56:127-36.
50. Stecksén-Blicks C, Granström E, Silfverdal SA, West CE. Prevalence of oral Candida in the first year of life. Mycoses. 2015;58:550-6.
51. Kleinegger CL, Lockhart SR, Vargas K, Soll DR. Frequency, intensity, species, and strains of oral Candida vary as a function of host age. J Clin Microbiol. 1996;34:2246-54.
52. Russell C, Lay KM. Natural history of Candida species and yeasts in the oral cavities of infants. Arch Oral Biol. 1973;18:957-62.
53. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010;6, e1000713.
54. Dupuy AK, David MS, Li L, Heider TN, Peterson JD, Montano EA, 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, e90899.
55. Ardissone AN, de la Cruz DM, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One. 2014;9, e90784.
56. La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci U S A. 2014;111:12522-7.
57. Moles L, Gómez M, Jiménez E, Fernández L, Bustos G, Chaves F, et al. Preterm infant gut colonization in the neonatal ICU and complete restoration 2 years later. Clin Microbiol Infect. 2015;21:936. e1-10.
58. Greenberg RG, Benjamin DK. Neonatal candidiasis: diagnosis, prevention, and treatment. J Infect. 2014;69 Suppl 1:S19-22.
59. Kumar S, Singhi S. Role of probiotics in prevention of Candida colonization and invasive candidiasis. J Matern Fetal Neonatal Med. 2016;29:818-9.
60. Manzoni P, Mostert M, Castagnola E. Update on the management of Candida infections in preterm neonates. Arch Dis Child Fetal Neonatal Ed. 2015;100:F454-9.
61. Kaufman DA, Gurka MJ, Hazen KC, Boyle R, Robinson M, Grossman LB. Patterns of fungal colonization in preterm infants weighing less than 1000 grams at birth. Pediatr Infect Dis J. 2006;25:733-7.
62. Gibson MK, Wang B, Ahmadi S, Burnham C-AD, Tarr PI, Warner BB, et al. Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome. Nat Microbiol. 2016;1:16024.
63. Langdon A, Crook N, Dantas G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med. 2016;8:39.
64. Yassour M, Vatanen T, Siljander H, Hämäläinen A-M, Härkönen T, Ryhänen SJ, et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016;8:343ra81.
65. Dollive S, Chen Y-Y, Grunberg S, Bittinger K, Hoffmann C, Vandivier L, et al. Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. PLoS One. 2013;8, e71806.
66. Kelly MS, Benjamin DK, Smith PB. The epidemiology and diagnosis of invasive Candidiasis among premature infants. Clin Perinatol. 2015;42:105-17.
67. Achkar JM, Fries BC. Candida infections of the genitourinary tract. Clin Microbiol Rev. 2010;23:253-73.
68. Shankar J, Solis NV, Mounaud S, Szpakowski S, Liu H, Losada L, et al. Using Bayesian modelling to investigate factors governing antibiotic-induced Candida albicans colonization of the GI tract. Sci Rep. 2015;5:8131.
69. Helstrom PB, Balish E. Effect of oral tetracycline, the microbial flora, and the athymic state on gastrointestinal colonization and infection of BALB/c mice with Candida albicans. Infect Immun. 1979;23:764-74.
70. Mason KL, Erb Downward JR, Mason KD, Falkowski NR, Eaton KA, Kao JY, et al. Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun. 2012;80:3371-80.
71. Leung MHY, Chan KCK, Lee PKH. Skin fungal community and its correlation with bacterial community of urban Chinese individuals. Microbiome. 2016;4:46.
72. Mukherjee PK, Chandra J, Retuerto M, Sikaroodi M, Brown RE, Jurevic R, et al. Oral mycobiome analysis of HIV-infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog. 2014;10, e1003996.
73. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480-4.
74. Bailey L, Forrest CB, Zhang P, Richards TM, Livshits A, DeRusso PA. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 2014;168:1063-9.
75. Riva A, Borgo F, Lassandro C, Verduci E, Morace G, Borghi E, et al. Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ Microbiol. 2016. doi: 10.1111/1462-2920.13463.
76. Borgo F, Verduci E, Riva A, Lassandro C, Riva E, Morace G, et al. Relative abundance in bacterial and fungal gut microbes in obese children: A case control study. Child Obes. 2016. Ahead of print.
77. Everard A, Matamoros S, Geurts L, Delzenne NM, Cani PD. Saccharomyces boulardii administration changes gut microbiota and reduces hepatic steatosis, low-grade inflammation, and fat mass in obese and type 2 diabetic db/db mice. MBio. 2014;5:e01011-4.
78. de Araújo TV, Andrade EF, Lobato RV, Orlando DR, Gomes NF, de Sousa RV, et al. Effects of beta-glucans ingestion (Saccharomyces cerevisiae) on metabolism of rats receiving high-fat diet. J Anim Physiol Anim Nutr. 2016. doi: 10.1111/jpn.12452.
79. Neyrinck AM, Possemiers S, Verstraete W, De Backer F, Cani PD, Delzenne NM. Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice. J Nutr Biochem. 2012;23:51-9.
80. Nicolosi R, Bell SJ, Bistrian BR, Greenberg I, Forse RA, Blackburn GL. Plasma lipid changes after supplementation with beta-glucan fiber from yeast. Am J Clin Nutr. 1999;70:208-12.
81. Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;7:307ra152.
82. Behbod B, Sordillo JE, Hoffman EB, Datta S, Webb TE, Kwan DL, et al. Asthma & allergy development: contrasting influences of yeasts & other fungal exposures. Clin Exp Allergy J. 2015;45:154-63.
83. World Health Organization. Diarrhoeal disease. http://www.who.int/mediacentre/factsheets/fs330/en/.
84. Kelesidis T, Pothoulakis C. Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Ther Adv Gastroenterol. 2012;5:111-25.
85. Feizizadeh S, Salehi-Abargouei A, Akbari V. Efficacy and safety of Saccharomyces boulardii for acute diarrhea. Pediatrics. 2014;134:e176-91.
86. Szajewska H, Mrukowicz J. Meta-analysis: non-pathogenic yeast Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea. Aliment Pharmacol Ther. 2005;22:365-72.
87. Szajewska H, Canani RB, Guarino A, Hojsak I, Indrio F, Kolacek S, et al. Probiotics for the prevention of antibiotic-associated diarrhea in children. J Pediatr Gastroenterol Nutr. 2016;62:495-506.
88. Chehoud C, Albenberg LG, Judge C, Hoffmann C, Grunberg S, Bittinger K, et al. Fungal signature in the gut microbiota of pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21:1948-56.
89. Mukhopadhya I, Hansen R, Meharg C, Thomson JM, Russell RK, Berry SH, et al. The fungal microbiota of de-novo paediatric inflammatory bowel disease. Microbes Infect. 2015;17:304-10.
90. Sokol H, Leducq V, Aschard H, Pham H-P, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2016. doi: 10.1136/gutjnl-2015-310746.
91. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, et al. Interactions between commensal fungi and the C-type lectin receptor dectin-1 influence colitis. Science. 2012;336:1314-7.
92. Osborne M, Reponen T, Adhikari A, Cho S-H, Grinshpun SA, Levin L, et al. Specific fungal exposures, allergic sensitization, and rhinitis in infants. Pediatr Allergy Immunol. 2006;17:450-7.
93. Szajewska H, Skórka A, Dylag M. Meta-analysis: Saccharomyces boulardii for treating acute diarrhoea in children. Aliment Pharmacol Ther. 2007;25:257-64.