The first fungi: mode of delivery determines early life fungal colonization in the intestine of preterm infants

Jannie G. E. Henderickx , Heleen de Weerd , Liesbeth J. Groot Jebbink , Diny van Zoeren-Grobben , Marieke A. C. Hemels , Richard A. van Lingen , Jan Knol , Clara Belzer

Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (1) : 7

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Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (1) :7 DOI: 10.20517/mrr.2021.03
Original Article

The first fungi: mode of delivery determines early life fungal colonization in the intestine of preterm infants

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Abstract

Aim: The role of intestinal fungi in human health and disease is becoming more evident. The mycobiota composition and diversity of preterm infants is affected by interactions with bacteria and clinical variables. In this study, we aimed to characterize the composition and the diversity of the preterm infant mycobiota and the effect of clinical variables on it in the first six postnatal weeks.

Methods: Preterm infants (n = 50) and full-term infants (n = 6) admitted to Isala Women and Children’s hospital (Zwolle, The Netherlands) who were born during 24-36 or 37-40 weeks of gestation, respectively, were included in this study. Feces were collected during the first six postnatal weeks (n = 109) and their mycobiota composition and diversity were characterized by ITS2 amplicon sequencing.

Results: Composition analyses identified fungi and other eukaryotic kingdoms, of which Viridiplantae was most abundant. Of the fungal kingdom, Ascomycota and Basidiomycota were the first and second most prominent phyla in early life of all infants. Candida was the most abundant genus in the first six weeks of life and increased with gestational and postnatal age. Fungal phylogenetic diversity remained stable in the first six postnatal weeks. The individuality and the mode of delivery were identified as significant predictors for the variation in the mycobiota composition. Vaginally delivered infants were enriched in Candida spp., whereas infants delivered through emergency C-section were characterized by Malassezia spp.

Conclusion: These results indicate that fungi and other eukaryotic kingdoms are detected in the intestine of preterm and full-term infants in the first six postnatal weeks. Similar to the microbiota, colonization of the preterm intestine with fungi is determined by clinical variables including individuality and mode of delivery.

Keywords

Intestinal tract / gut / fungi / mycobiota / premature birth / infant

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Jannie G. E. Henderickx, Heleen de Weerd, Liesbeth J. Groot Jebbink, Diny van Zoeren-Grobben, Marieke A. C. Hemels, Richard A. van Lingen, Jan Knol, Clara Belzer. The first fungi: mode of delivery determines early life fungal colonization in the intestine of preterm infants. Microbiome Research Reports, 2022, 1(1): 7 DOI:10.20517/mrr.2021.03

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References

[1]

Chin VK,Chong PP,Basir R.Mycobiome in the gut: a multiperspective review.Mediators Inflamm2020;2020:9560684 PMCID:PMC7160717

[2]

Manor O,Kornilov SA.Health and disease markers correlate with gut microbiome composition across thousands of people.Nat Commun2020;11:5206 PMCID:PMC7562722

[3]

Lynch SV.The human intestinal microbiome in health and disease.N Engl J Med2016;375:2369-79

[4]

Fan Y.Gut microbiota in human metabolic health and disease.Nat Rev Microbiol2021;19:55-71

[5]

Pfeiffer JK.Viral immunity. Transkingdom control of viral infection and immunity in the mammalian intestine.Science2016;351:aad5872 PMCID:PMC4751997

[6]

Schei K,Øien T.Early gut mycobiota and mother-offspring transfer.Microbiome2017;5:107 PMCID:PMC5571498

[7]

Bliss JM,Watson WJ,Ryan RM.Vertical and horizontal transmission of Candida albicans in very low birth weight infants using DNA fingerprinting techniques.Pediatr Infect Dis J2008;27:231-5

[8]

Ward TL,Heisel T,Knights D.Development of the human mycobiome over the first month of life and across body sites.mSystems2018;3:e00140-17 PMCID:PMC5840654

[9]

Ward TL,Gale CA.Infant fungal communities: current knowledge and research opportunities.BMC Med2017;15:30 PMCID:PMC5304398

[10]

Strati F,Stefanini I.Age and gender affect the composition of fungal population of the human gastrointestinal tract.Front Microbiol2016;7:1227 PMCID:PMC4971113

[11]

James SA,Telatin A.Preterm infants harbour a rapidly changing mycobiota that includes Candida pathobionts.J Fungi (Basel)2020;6:273 PMCID:PMC7712117

[12]

Mason KL,Mason KD.Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy.Infect Immun2012;80:3371-80 PMCID:PMC3457555

[13]

Filyk HA.The multibiome: the intestinal ecosystem’s influence on immune homeostasis, health, and disease.EBioMedicine2016;13:46-54 PMCID:PMC5264270

[14]

LaTuga MS,Cotton CM.Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants.PLoS One2011;6:e27858 PMCID:PMC3234235

[15]

Underhill DM.The mycobiota: interactions between commensal fungi and the host immune system.Nat Rev Immunol2014;14:405-16 PMCID:PMC4332855

[16]

Moré MI.Saccharomyces boulardii CNCM I-745 supports regeneration of the intestinal microbiota after diarrheic dysbiosis - a review.Clin Exp Gastroenterol2015;8:237-55 PMCID:PMC4542552

[17]

Zanello G,Berri M.Saccharomyces boulardii effects on gastrointestinal diseases.Curr Issues Mol Biol2009;11:47-58.

[18]

Greenberg RG.Neonatal candidiasis: diagnosis, prevention, and treatment.J Infect2014;69 Suppl 1:S19-22 PMCID:PMC4252884

[19]

Benjamin DK Jr,Fanaroff AA.National Institute of Child Health and Human Development Neonatal Research NetworkNeonatal candidiasis among extremely low birth weight infants: risk factors, mortality rates, and neurodevelopmental outcomes at 18 to 22 months.Pediatrics2006;117:84-92

[20]

Henderickx JGE,Renes IB.Maturation of the preterm gastrointestinal tract can be defined by host and microbial markers for digestion and barrier defense.Sci Rep2021;11:12808 PMCID:PMC8211855

[21]

Zwittink RD,Martin R.Metaproteomics reveals functional differences in intestinal microbiota development of preterm infants.Mol Cell Proteomics2017;16:1610-20 PMCID:PMC5587861

[22]

Zwittink RD,Renes IB.Dynamics of the bacterial gut microbiota in preterm and term infants after intravenous amoxicillin/ceftazidime treatment.BMC Pediatr2020;20:195 PMCID:PMC7204001

[23]

Zwittink RD,van Lingen RA.Association between duration of intravenous antibiotic administration and early-life microbiota development in late-preterm infants.Eur J Clin Microbiol Infect Dis2018;37:475-83 PMCID:PMC5816780

[24]

Stecher G,Kumar S.Molecular evolutionary genetics analysis (MEGA) for macOS.Mol Biol Evol2020;37:1237-9

[25]

Rivers AR. Q2-ITSxpress: a tutorial on a QIIME 2 plugin to trim ITS sequences. Available from: https://forum.qiime2.org/t/q2-itsxpress-a-tutorial-on-a-qiime-2-plugin-to-trim-its-sequences/5780 [Last accessed on 18 Jan 2022]

[26]

Rivers AR,Gardner TG,Armstrong SD.ITSxpress: software to rapidly trim internally transcribed spacer sequences with quality scores for marker gene analysis.F1000Res2018;7:1418 PMCID:PMC6206612

[27]

Nilsson RH,Abarenkov K,Kristiansson E.The ITS region as a target for characterization of fungal communities using emerging sequencing technologies.FEMS Microbiol Lett2009;296:97-101

[28]

Callahan BJ,Rosen MJ,Johnson AJ.DADA2: high-resolution sample inference from Illumina amplicon data.Nat Methods2016;13:581-3 PMCID:PMC4927377

[29]

Abarenkov K,Piirmann T.UNITE QIIME release for eukaryotes.2021;

[30]

R Core Team. R: a language and environment for statistical computing. Available from: https://www.r-project.org/ [Last accessed on 18 Jan 2022]

[31]

Bisanz JE. qiime2R: importing QIIME2 artifacts and associated data into R sessions. Available from: https://github.com/jbisanz/qiime2R [Last accessed on 18 Jan 2022]

[32]

Lahti L.microbiome R package.Bioconductor2017;

[33]

Wickham H.ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2016.

[34]

Kassambara A. ggpubr: “ggplot2” based publication ready plots. Available from: https://rpkgs.datanovia.com/ggpubr/ [Last accessed on 18 Jan 2022]

[35]

Revelle W. psych: procedures for psychological, psychometric, and personality research. Available from: https://cran.r-project.org/package=psych [Last accessed on 18 Jan 2022]

[36]

McMurdie PJ.phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.PLoS One2013;8:e61217 PMCID:PMC3632530

[37]

Galili T.dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering.Bioinformatics2015;31:3718-20 PMCID:PMC4817050

[38]

Kembel SW,Helmus MR.Picante: R tools for integrating phylogenies and ecology.Bioinformatics2010;26:1463-4

[39]

Oksanen J,Friendly M. vegan: community ecology package. Available from: https://cran.r-project.org/package=vegan [Last accessed on 18 Jan 2022]

[40]

Aitchison J,Martín-Fernández JA.Logratio analysis and compositional distance.Math Geol2000;32:271-5

[41]

Quinn TP,Richardson MF.Understanding sequencing data as compositions: an outlook and review.Bioinformatics2018;34:2870-8 PMCID:PMC6084572

[42]

Rrumen. Available from: https://github.com/seashore001x/Rrumen/blob/master/phyloseq2lefse.R [Last accessed on 18 Jan 2022]

[43]

Pandey PK,Verma P,Patole MS.Molecular typing of fecal eukaryotic microbiota of human infants and their respective mothers.J Biosci2012;37:221-6

[44]

Greenberg JA,Van Ausdal W.Omega-3 fatty acid supplementation during pregnancy.Rev Obstet Gynecol2008;1:162-9 PMCID:PMC2621042

[45]

von Schacky C.Omega-3 fatty acids in pregnancy-the case for a target Omega-3 index.Nutrients2020;12:898 PMCID:PMC7230742

[46]

Richard ML.The gut mycobiota: insights into analysis, environmental interactions and role in gastrointestinal diseases.Nat Rev Gastroenterol Hepatol2019;16:331-45

[47]

Cotten CM,Stoll B,Poole K.National Institute for Child Health and Human Development Neonatal Research NetworkThe association of third-generation cephalosporin use and invasive candidiasis in extremely low birth-weight infants.Pediatrics2006;118:717-22

[48]

Saiman L,Pfaller M.Risk factors for candidemia in Neonatal Intensive Care Unit patients. The National Epidemiology of Mycosis Survey study group.Pediatr Infect Dis J2000;19:319-24

[49]

Barton M,Robinson JL.Invasive candidiasis in low birth weight preterm infants: risk factors, clinical course and outcome in a prospective multicenter study of cases and their matched controls.BMC Infect Dis2014;14:327 PMCID:PMC4063435

[50]

Kelly MS,Smith PB.The epidemiology and diagnosis of invasive candidiasis among premature infants.Clin Perinatol2015;42:105-17, viii PMCID:PMC4328135

[51]

Ali GY,Rashed KA,Khalifa AA.Prevalence of Candida colonization in preterm newborns and VLBW in neonatal intensive care unit: role of maternal colonization as a risk factor in transmission of disease.J Matern Fetal Neonatal Med2012;25:789-95

[52]

Kaufman D.“Getting to Zero”: preventing invasive Candida infections and eliminating infection-related mortality and morbidity in extremely preterm infants.Early Human Development2012;88:S45-9

[53]

Pappas PG,Arendrup MC,Kullberg BJ.Invasive candidiasis.Nat Rev Dis Primers2018;4:18026

[54]

Çerikçioǧlu N,Bilgen H,Metin F.The relationships between candidemia and candidal colonization and virulence factors of the colonizing strains in preterm infants.Turk J Pediatr2004;46:245-50

[55]

Coates EW,Croitoru DP.Distinctive distribution of pathogens associated with peritonitis in neonates with focal intestinal perforation compared with necrotizing enterocolitis.Pediatrics2005;116:e241-6

[56]

Parra-Herran CE,Sola JE,Rodriguez MM.Intestinal candidiasis: an uncommon cause of necrotizing enterocolitis (NEC) in neonates.Fetal Pediatr Pathol2010;29:172-80

[57]

Tso GHW,Tan ASM.Experimental evolution of a fungal pathogen into a gut symbiont.Science2018;362:589-95

[58]

Heisel T,Sadowsky MJ.Breastmilk and NICU surfaces are potential sources of fungi for infant mycobiomes.Fungal Genet Biol2019;128:29-35 PMCID:PMC6555646

[59]

Boix-Amorós A,du Toit E.Mycobiome profiles in breast milk from healthy women depend on mode of delivery, geographic location, and interaction with bacteria.Appl Environ Microbiol2019;85:e02994-18 PMCID:PMC6495746

[60]

Findley K,Yang J.NIH Intramural Sequencing Center Comparative Sequencing ProgramTopographic diversity of fungal and bacterial communities in human skin.Nature2013;498:367-70 PMCID:PMC3711185

[61]

Nagata R,Ogishima D,Hiruma M.Transmission of the major skin microbiota, Malassezia, from mother to neonate.Pediatr Int2012;54:350-5

[62]

Dominguez-Bello MG,Contreras M.Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.Proc Natl Acad Sci U S A2010;107:11971-5 PMCID:PMC2900693

[63]

Qin J,Raes J.MetaHIT ConsortiumA human gut microbial gene catalogue established by metagenomic sequencing.Nature2010;464:59-65 PMCID:PMC3779803

[64]

Sender R,Milo R.Revised estimates for the number of human and bacteria cells in the body.PLoS Biol2016;14:e1002533 PMCID:PMC4991899

[65]

Tiew PY,Ali NABM.The Mycobiome in health and disease: emerging concepts, methodologies and challenges.Mycopathologia2020;185:207-31 PMCID:PMC7223441

[66]

Mac Aogáin M,Chotirmall SH.MycopathologiaGENOMES: the new ‘home’ for the publication of fungal genomes.Mycopathologia2019;184:551-4

[67]

Gabaldón T.Consortium OPATHYRecent trends in molecular diagnostics of yeast infections: from PCR to NGS.FEMS Microbiol Rev2019;43:517-47 PMCID:PMC8038933

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