Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life

Boutin, Rozlyn C.T.; Petersen, Charisse; Woodward, Sarah E.; Serapio-Palacios, Antonio; Bozorgmehr, Tahereh; Loo, Rachelle; Chalanuchpong, Alina; Cirstea, Mihai; Lo, Bernard C.; Huus, Kelsey E.; Barcik, Weronika; Azad, Meghan B.; Becker, Allan B.; Mandhane, Piush J.; Moraes, Theo J.; Sears, Malcolm R.; Subbarao, Padmaja; McNagny, Kelly M.; Turvey, Stuart E.; Finlay, B. Brett

doi:10.7554/elife.67740

Cited by 28 publications

(30 citation statements)

References 79 publications

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“…Recently, a study established a link between bacterial-fungal interactions in the neonatal gut involving SCFA production and asthma development. 88 This research follows a previous article, which demonstrated that, in addition to bacterial dysbiosis, fungal dysbiosis in the gut of 3-month-old Ecuadorian infants increases the risk of developing asthma at 5 years of age. 89 This fungal dysbiosis is characterized by a general increase in the fungal population in the gut and, more particularly, an increased abundance of Pichia kudriavzevii (also known as Candida krusei ).…”

Section: Gut Short Chain Fatty Acids Involvement In the Bacterial-fun...supporting

confidence: 65%

Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review

Lapière

Richard

2022

Gut Microbes

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The composition of the microbiota is the focus of many recent publications describing the effects of the microbiota on host health. In recent years, research has progressed further, investigating not only the diversity of genes and functions but also metabolites produced by microorganisms composing the microbiota of various niches and how these metabolites affect and shape the microbial community. While an abundance of data has been published on bacterial interactions, much less data are available on the interactions of bacteria with another component of the microbiota: the fungal community. Although present in smaller numbers, fungi are essential to the balance of this complex microbial ecosystem. Both bacterial and fungal communities produce metabolites that influence their own population but also that of the other. However, to date, interkingdom interactions occurring through metabolites produced by bacteria and fungi have rarely been described. In this review, we describe the major metabolites produced by both kingdoms and discuss how they influence each other, by what mechanisms and with what consequences for the host.

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Section: Gut Short Chain Fatty Acids Involvement In the Bacterial-fun...supporting

confidence: 65%

Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review

Lapière

Richard

2022

Gut Microbes

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“…Pichia , a member of the oral and gut microbiome 40 , was shown to be increased in Clostridium difficile infection when compared to healthy individuals 41 and has implicated in infant gut mycobial dysbiosis associated with atopic disease 42 . P. kudriavzevii belonging to Pichia genus was associated with an increased inflammatory response and a reduced abundance of short chain fatty acids (SCFAs) in mice 43 . It was shown that the gut dysbiosis with depletion in SCFA-producing bacteria, which characterizes GDM patients 44 , can increase the predominance of inflammatory fungal taxa, such as Pichia , that release an inhibitory molecule with antagonistic effects against the other fungi 40 , thus explaining its increased relative frequency in the GDM patients.…”

Section: Discussionmentioning

confidence: 99%

Mycobiota composition and changes across pregnancy in patients with gestational diabetes mellitus (GDM)

Ferrocino

Ponzo

Pellegrini

et al. 2022

Sci Rep

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The gut mycobiota has never been studied either during pregnancy or in patients with gestational diabetes (GDM). This study aimed to analyze the fecal mycobiota of GDM patients during the second (T2) and third (T3) trimester of pregnancy and to compare it with the mycobiota of pregnant normoglycemic women (controls). Forty-one GDM patients and 121 normoglycemic women were studied. GDM mycobiota was composed almost exclusively by the Ascomycota phylum; Basidiomicota accounted for 43% of the relative frequency of the controls. Kluyveromyces (p < 0.001), Metschnikowia (p < 0.001), and Pichia (p < 0.001) showed a significantly higher frequency in GDM patients, while Saccharomyces (p = 0.019), were more prevalent in controls. From T2 to T3, a reduction in fungal alpha diversity was found in GDM patients, with an increase of the relative frequency of Candida, and the reduction of some pro-inflammatory taxa. Many associations between fungi and foods and nutrients were detected. Finally, several fungi and bacteria showed competition or co-occurrence. Patients with GDM showed a predominance of fungal taxa with potential inflammatory effects when compared to normoglycemic pregnant women, with a marked shift in their mycobiota during pregnancy, and complex bacteria-fungi interactions.

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“…Similar investigations for associations in the infant gut have not yet been described, but emerging research in animals reveals a role for early life interkingdom interactions in long-term health outcomes. For example, Boutin and colleagues found that fungi interact with bacteria in the neonatal murine gut (via bacterially derived short chain fatty acids) to influence the severity of allergic airway disease later in life (Boutin et al, 2021a). This study focused on the analysis of microbiomes and mycobiomes of mother-infant dyads who were involved in exclusive breastfeeding.…”

Section: Discussionmentioning

confidence: 99%

Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

et al. 2022

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The composition and function of early life gut bacterial communities (microbiomes) have been proposed to modulate health for the long term. In addition to bacteria, fungi (mycobiomes) also colonize the early life gut and have been implicated in health disorders such as asthma and obesity. Despite the potential importance of mycobiomes in health, there has been a lack of study regarding fungi and their interkingdom interactions with bacteria during infancy. The goal of this study was to obtain a more complete understanding of microbial communities thought to be relevant for the early life programming of health. Breastmilk and infant feces were obtained from a unique cohort of healthy, exclusively breastfeeding dyads recruited as part of the Mothers and Infants Linked for Healthy Growth (MILk) study with microbial taxa characterized using amplicon-based sequencing approaches. Bacterial and fungal communities in breastmilk were both distinct from those of infant feces, consistent with niche-specific microbial community development. Nevertheless, overlap was observed among sample types (breastmilk, 1-month feces, 6-month feces) with respect to the taxa that were the most prevalent and abundant. Self-reported antibacterial antibiotic exposure was associated with micro- as well as mycobiome variation, which depended upon the subject receiving antibiotics (mother or infant), timing of exposure (prenatal, peri- or postpartum), and sample type. In addition, birth mode was associated with bacterial and fungal community variation in infant feces, but not breastmilk. Correlations between bacterial and fungal taxa abundances were identified in all sample types. For infant feces, congruency between bacterial and fungal communities was higher for older infants, consistent with the idea of co-maturation of bacterial and fungal gut communities. Interkingdom connectedness also tended to be higher in older infants. Additionally, higher interkingdom connectedness was associated with Cesarean section birth and with antibiotic exposure for microbial communities of both breastmilk and infant feces. Overall, these results implicate infant age, birth mode, and antibiotic exposure in bacterial, fungal and interkingdom relationship variation in early-life-relevant microbiomes, expanding the current literature beyond bacteria.

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Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life

Cited by 28 publications

References 79 publications

Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review

Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review

Mycobiota composition and changes across pregnancy in patients with gestational diabetes mellitus (GDM)

Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

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