Minority species influences microbiota formation: the role of Bifidobacterium with extracellular glycosidases in bifidus flora formation in breastfed infant guts

Abstract

Summary The human body houses a variety of microbial ecosystems, such as the microbiotas on the skin, in the oral cavity and in the digestive tract. The gut microbiota is one such ecosystem that contains trillions of bacteria, and it is well established that it can significantly influence host health and diseases. With the advancement in bioinformatics tools, numerous comparative studies based on 16S ribosomal RNA ( rRNA ) gene sequences, metabolomics, pathological and epidemical analyses have revealed the correlative relationship between the abundance of certain taxa and disease states or amount of certain causative bioactive compounds. However, the 16S rRNA ‐based taxonomic analyses using next‐generation sequencing ( NGS ) technology essentially detect only the majority species. Although the entire gut microbiome consists of 10 13 microbial cells, NGS read counts are given in multiples of 10 6 , making it difficult to determine the diversity of the entire microbiota. Some recent studies have reported instances where certain minority species play a critical role in creating locally stable conditions for other species by stabilizing the fundamental microbiota, despite their low abundance. These minority species act as ‘keystone species’, which is a species whose effect on the community is disproportionately large compared to its relative abundance. One of the attributes of keystone species within the gut microbiota is its extensive enzymatic capacity for substrates that are rare or difficult to degrade for other species, such as dietary fibres or host‐derived complex glycans, like human milk oligosaccharides ( HMO s). In this paper, we propose that more emphasis should be placed on minority taxa and their possible role as keystone species in gut microbiota studies by referring to our recent studies on HMO ‐mediated microbiota formation in the infant gut.

Next Generation Microbiome Research: Identification of Keystone Species in the Metabolic Regulation of Host-Gut Microbiota Interplay

“…Degradation of complex carbohydrates (arabinogalactan); selective BSH activity (Yao et al, 2018) Empirical (Cartmell et al, 2018) Unclear -Controversial association with IBD (Sitkin and Pokrotnieks, 2019) Bifidobacterium longum Degradation of complex carbohydrates, particularly Human Milk Oligosaccharides; BSH activity (Tanaka et al, 2000) Empirical (Yu et al, 2013;Gotoh et al, 2019) Highly prevalent in healthy newborns (Favier et al, 2003) Bifidobacterium pseudolongum…”

Butyrate producing colonic Clostridiales metabolise human milk oligosaccharides and cross feed on mucin via conserved pathways

“…Dietary glycans resistant to digestion by human enzymes are a major driver that shapes the developing HGM 6,15 . This is emphasized by the dominance of Bifidobacterium in breast-fed infants 7,8 , attributed to the competitiveness of distinct members of this genus in the utilization of human milk oligosaccharides (HMOs) 16,17 . Indeed, the most prominent changes in the infant microbiota occur during weaning and the introduction of solid food 6,7 , whereby bifidobacteria are replaced by Firmicutes as the top abundant phylum of the mature HGM.…”

Bovine Teat Cistern Microbiota Composition and Richness Are Associated With the Immune and Microbial Responses During Transition to Once-Daily Milking

“…Rare species can drive key processes in ecosystem functioning and stability and they represent a reservoir of genes, allowing adaptation to changing conditions and, as a result, resilience of the ecosystem function ( Jousset et al, 2017 ). They can affect community assembly through metabolic interaction by supporting the growth of dominant species ( Gotoh et al, 2019 ) and contribute to host health by preventing the invasion of new species through “colonization resistance” ( Mallon et al, 2015 ). Likewise, by increasing the range of interactions with the host, rare species probably contribute to the interaction with the immune system (stimulation/inhibition) ( Stecher et al, 2013 ; Jousset et al, 2017 ).…”