Human milk fungi: environmental determinants and inter-kingdom associations with milk bacteria in the CHILD Cohort Study

Shirin Moossavi,Piushkumar J Mandhane,Padmaja Subbarao,Malcolm R Sears,Stuart E Turvey,Hooman Derakhshani,Theo J Moraes,Jeffrey Brook,Kelsey Fehr,Allan B Becker,Ehsan Khafipour,Meghan B Azad,Hind Sbihi,Bianca Robertson,Lars Bode

doi:10.1186/s12866-020-01829-0

Abstract

BackgroundFungi constitute an important yet frequently neglected component of the human microbiota with a possible role in health and disease. Fungi and bacteria colonise the infant gastrointestinal tract in parallel, yet most infant microbiome studies have ignored fungi. Milk is a source of diverse and viable bacteria, but few studies have assessed the diversity of fungi in human milk.ResultsHere we profiled mycobiota in milk from 271 mothers in the CHILD birth cohort and detected fungi in 58 (21.4%). Samples containing detectable fungi were dominated by Candida, Alternaria, and Rhodotorula, and had lower concentrations of two human milk oligosaccharides (disialyllacto-N-tetraose and lacto-N-hexaose). The presence of milk fungi was associated with multiple outdoor environmental features (city, population density, and season), maternal atopy, and early-life antibiotic exposure. In addition, despite a strong positive correlation between bacterial and fungal richness, there was a co-exclusion pattern between the most abundant fungus (Candida) and most of the core bacterial genera.ConclusionWe profiled human milk mycobiota in a well-characterised cohort of mother-infant dyads and provide evidence of possible host-environment interactions in fungal inoculation. Further research is required to establish the role of breastfeeding in delivering fungi to the developing infant, and to assess the health impact of the milk microbiota in its entirety, including both bacterial and fungal components.

Highlights

Fungi constitute an important yet frequently neglected component of the human microbiota with a possible role in health and disease
Presence of milk fungi was significantly and independently associated with environmental characteristics, human milk oligosaccharides, and milk bacterial composition Using a minimum threshold of 1000 reads/sample informed by positive PCR results (Fig. 1a), 58/271 (21.4%) of mothers’ milk samples contained fungi
Milk microbiota composition differs in the presence vs. absence of breastmilk fungi Since we observed that bacterial taxonomic clusters were associated with fungi presence (Figs. 2a & 4a), we further explored the relationship between milk bacteria and mycobiota

Summary

Introduction

Fungi constitute an important yet frequently neglected component of the human microbiota with a possible role in health and disease. Milk is a source of diverse and viable bacteria, but few studies have assessed the diversity of fungi in human milk. Fungi constitute an important yet frequently neglected component of the human microbiome [1, 2] with a possible role in health and disease [3, 4]. Milk is a source of diverse and viable bacteria [6], but only a few studies have assessed fungi in human milk [7,8,9,10,11,12]. Home characteristics and season are associated with indoor fungi [17, 18] and could plausibly influence milk mycobiota; mothers’ milk and the home environment (another potential source of milk fungi) have not been examined

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Discussion

Conclusion