Divergent maturational patterns of the infant bacterial and fungal gut microbiome in the first year of life are associated with inter-kingdom community dynamics and infant nutrition

Study information

Reviewed Marked as Reviewed by Svetlana up on 2024-4-8

study design

time series / longitudinal observational
prospective cohort

Citation

PMID PubMed identifier for scientific articles.

38326891

DOI Digital object identifier for electronic documents.

https://doi.org/10.1186/s40168-023-01735-3

URI

Authors

Mercer EM, Ramay HR, Moossavi S, Laforest-Lapointe I, Reyna ME, Becker AB, Simons E, Mandhane PJ, Turvey SE, Moraes TJ, Sears MR, Subbarao P, Azad MB, Arrieta MC

Journal

Microbiome

Year

2024

Keywords:

Alpha diversity, Colonization patterns, Early life, Gut fungi, Gut microbiome, Gut mycobiome, Inter-kingdom dynamics, Microbial succession, Microbiome maturation

BACKGROUND: The gut microbiome undergoes primary ecological succession over the course of early life before achieving ecosystem stability around 3 years of age. These maturational patterns have been well-characterized for bacteria, but limited descriptions exist for other microbiota members, such as fungi. Further, our current understanding of the prevalence of different patterns of bacterial and fungal microbiome maturation and how inter-kingdom dynamics influence early-life microbiome establishment is limited. RESULTS: We examined individual shifts in bacterial and fungal alpha diversity from 3 to 12 months of age in 100 infants from the CHILD Cohort Study. We identified divergent patterns of gut bacterial or fungal microbiome maturation in over 40% of infants, which were characterized by differences in community composition, inter-kingdom dynamics, and microbe-derived metabolites in urine, suggestive of alterations in the timing of ecosystem transitions. Known microbiome-modifying factors, such as formula feeding and delivery by C-section, were associated with atypical bacterial, but not fungal, microbiome maturation patterns. Instead, fungal microbiome maturation was influenced by prenatal exposure to artificially sweetened beverages and the bacterial microbiome, emphasizing the importance of inter-kingdom dynamics in early-life colonization patterns. CONCLUSIONS: These findings highlight the ecological and environmental factors underlying atypical patterns of microbiome maturation in infants, and the need to incorporate multi-kingdom and individual-level perspectives in microbiome research to improve our understandings of gut microbiome maturation patterns in early life and how they relate to host health. Video Abstract.

Experiment 1

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Reviewed Marked as Reviewed by Svetlana up on 2024-4-8

Curated date: 2024/03/15

Curator: Tayk26

Revision editor(s): Tayk26, Svetlana up

Subjects

Location of subjects: Canada

Host species Species from which microbiome was sampled. Contact us to have more species added.: Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Gut microbiome measurement Gut microbiome measurement,gut microbiome measurement

Group 0 name Corresponds to the control (unexposed) group for case-control studies: 3 months

Group 1 name Corresponds to the case (exposed) group for case-control studies: 12 months

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: infants when they are 12 months of age

Group 0 sample size Number of subjects in the control (unexposed) group: 99

Group 1 sample size Number of subjects in the case (exposed) group: 99

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): exposure prior to 3 months

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance: Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).: raw counts

Statistical test: DESeq2

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.001

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?: Yes

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness: increased

Chao1 Abundance-based estimator of species richness: increased

Signature 1

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Curated date: 2024/03/23

Curator: Tayk26

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Source: Fig 3C

Description: Comparison of bacterial growth at 3 and 12 months

Abundance in Group 1: increased abundance in 12 months

NCBI	Quality Control	Links
Akkermansia muciniphila
Bacteroides caccae
Bacteroides uniformis
Segatella copri
unclassified Rikenellaceae

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Signature 2

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Curated date: 2024/03/23

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Source: Fig 3C

Description: Comparison of bacterial growth at 3 and 12 months

Abundance in Group 1: decreased abundance in 12 months

NCBI	Quality Control	Links
Bacteroides ovatus
unclassified Bacteroides

Revision editor(s): Tayk26, Svetlana up

Experiment 2

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Curated date: 2024/03/23

Curator: Tayk26

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Differences from previous experiment shown

Subjects

Group 0 sample size Number of subjects in the control (unexposed) group: 95

Group 1 sample size Number of subjects in the case (exposed) group: 95

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): before 3 months