Unique ecology of co-occurring functionally and phylogenetically undescribed species in the infant oral microbiome

TL;DR

This study identifies two new bacterial species in infant mouths that work together, exchanging nutrients to support each other and possibly protect against tooth decay.

Contribution

Discovery of two novel co-occurring bacterial species in infant oral microbiomes and their predicted metabolic interactions.

Findings

Two novel Streptococcus and Rothia species are prevalent and co-occur in infant oral microbiomes.

The species exchange amino acids like ornithine and lysine, suggesting a cooperative metabolic relationship.

Genomic analysis reveals functional traits like adhesins and CAZymes that may aid colonization and nutrient processing.

Abstract

Early-life oral microbiome development is a complex community assembly process that influences long-term health outcomes. Nevertheless, microbial functions and interactions driving these ecological processes remain poorly understood. In this study, we analyze oral microbiomes from a longitudinal cohort of 24 mother-infant dyads at 1 and 6 months postpartum using shotgun metagenomics. We identify two previously undescribed Streptococcus and Rothia species to be among the most prevalent, abundant and strongly co-occurring members of the oral microbiome of six-month-old infants. By leveraging metagenome-assembled genomes (MAGs) and genome-scale metabolic models (GEMS) we reveal their genomic and functional characteristics relative to other infant-associated species and predict their metabolic interactions within a network of co-occurring oral taxa. Our findings highlight unique functional features, including genes encoding adhesins and carbohydrate-active enzymes (CAZymes). Metabolic modeling identified potential exchange of key amino acids, particularly ornithine and lysine, between these species, suggesting metabolic cross-feeding interactions that may explain their co-abundance across infant oral microbiomes. Overall, this study provides key insights into the functional adaptations and microbial interactions shaping early colonization in the oral cavity, providing testable hypotheses for future experimental validation.

We investigated how infant oral bacterial communities develop during their first six months of life, with the aim to understand which microbes colonize, how they establish themselves and why they succeed together. Using high throughput DNA sequencing techniques, we analyzed oral samples from 24 mother-infant pairs at one and six months after birth. We found two abundant, but previously unknown bacterial species (one Streptococcus spp. and one Rothia spp.) at six months of age. These bacteria consistently appear together across different babies, suggesting they may depend on each other for survival and growth. By reconstructing the genomes of these bacteria directly from our samples, we discovered specific genetic features that help explain their success in the infant mouth. Streptococcus carries genes involved in amino acid biosynthesis (including arginine biosynthesis using amino acids present in breast milk) as well as enzymes that help break down carbohydrates in the oral biofilm. Rothia has genes associated with cell membrane biosynthesis and carbohydrate metabolism, while producing nutrients that Streptococcus needs. We predict these bacteria exchange key nutrients like ornithine and lysine, creating a mutually beneficial partnership. The bacteria seem to cooperate and are predicted to exchange key nutrients like malate and lysine which may help maintain a healthy oral environment by regulating acidity levels, potentially protecting against tooth decay.

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