Early gut mycobiota and mother-offspring transfer

Kasper Schei, Ekaterina Avershina, Torbjørn Øien, Knut Rudi, Turid Follestad, Saideh Salamati, Rønnaug Astri Ødegård, Kasper Schei, Ekaterina Avershina, Torbjørn Øien, Knut Rudi, Turid Follestad, Saideh Salamati, Rønnaug Astri Ødegård

Abstract

Background: The fungi in the gastrointestinal tract, the gut mycobiota, are now recognised as a significant part of the gut microbiota, and they may be important to human health. In contrast to the adult gut mycobiota, the establishment of the early gut mycobiota has never been described, and there is little knowledge about the fungal transfer from mother to offspring.

Methods: In a prospective cohort, we followed 298 pairs of healthy mothers and offspring from 36 weeks of gestation until 2 years of age (1516 samples) and explored the gut mycobiota in maternal and offspring samples. Half of the pregnant mothers were randomised into drinking probiotic milk during and after pregnancy. The probiotic bacteria included Lactobacillus rhamnosus GG (LGG), Bifidobacterium animalis subsp. lactis Bb-12 and Lactobacillus acidophilus La-5. We quantified the fungal abundance of all the samples using qPCR of the fungal internal transcribed spacer (ITS)1 segment, and we sequenced the 18S rRNA gene ITS1 region of 90 high-quantity samples using the MiSeq platform (Illumina).

Results: The gut mycobiota was detected in most of the mothers and the majority of the offspring. The offspring showed increased odds of having detectable faecal fungal DNA if the mother had detectable fungal DNA as well (OR = 1.54, p = 0.04). The fungal alpha diversity in the offspring gut increased from its lowest at 10 days after birth, which was the earliest sampling point. The fungal diversity and fungal species showed a succession towards the maternal mycobiota as the child aged, with Debaryomyces hansenii being the most abundant species during breast-feeding and Saccharomyces cerevisiae as the most abundant after weaning. Probiotic consumption increased the gut mycobiota abundance in pregnant mothers (p = 0.01).

Conclusion: This study provides the first insight into the early fungal establishment and the succession of fungal species in the gut mycobiota. The results support the idea that the fungal host phenotype is transferred from mother to offspring.

Trial registration: Clinicaltrials.gov NCT00159523.

Keywords: Fungi; Gut microbiota; Infant; Infant health; Mycobiota; Newborn; Probiotics.

Conflict of interest statement

Ethics approval and consent to participate

This study was approved by the Regional Committee for Medical and Health Research Ethics for Central Norway (ref: 120-2000 and 2014/1796/REK midt) and the Norwegian Data Inspectorate (ref: 2003/953-3 KBE/-). At least one of each child’s parent was informed and signed an informed consent form.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Detection of fungal ITS DNA. The counts of samples with detected and non-detected fungal ITS DNA for each age group. The detection limit was set to a higher fungal ITS concentration than the negative control or within a CT value of 45 cycles
Fig. 2
Fig. 2
Fungal ITS DNA concentration in maternal and offspring faecal samples. A scatter plot of the fungal ITS DNA concentrations (log ITS copies per mL, mean and 95% CI). The concentration of the ITS copies quantifies the amounts of fungi in the samples
Fig. 3
Fig. 3
Alpha and beta diversity for the faecal samples. A scatter plot of the diversities; red whiskers designate the median and interquartile ranges. a Alpha diversity as Simpson’s reciprocal index. The Simpson reciprocal index describes how many OTUs prevail in each sample [36]. b The observed species index describes the sample richness, i.e. how many OTUs are detected in each sample. c The beta diversity as Bray-Curtis Distance describes the between-sample diversity from 0 to 1
Fig. 4
Fig. 4
a–c OTU abundances for all groups. Bar charts of the relatively most abundant OTUs in a mothers, b offspring from 10 days to 3 months and c offspring for 1–2 years. Each coloured box represents an OTU. The individual fungal ITS DNA concentration is on top of each bar
Fig. 5
Fig. 5
Overlapping OTUs between pregnant woman and their offspring. The counts of overlapping OTUs in five mother-offspring pairs from the sequencing of the 18S rRNA gene ITS1 regions

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