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Recent studies have suggested that the human gut microbiota (GM) is associated with behavioral and psychological phenotypes in infancy and childhood. Here, we aimed to understand the relationship between GM and temperament, a biological individual variation in emotional reactivity and regulation. Temperament is considered an important predictor of the later personality of an individual and the associated behavioral and mental health issues. Since GM reaches an adult-like composition in the 3–5 years after birth, we hypothesized that the maturity of GM compositions in this period would relate to some specific temperament traits.
We analyzed 284 Japanese children (mean age = 46.44 ± 6.27 months) and evaluated their GM via 16S rRNA sequencing of stool samples. We examined alpha diversity, the diversity of bacteria within the individual, through a principal component analysis of four indices—Shannon diversity, Chao1, Observed species, and Faith’s phylogenetic diversity. We also examined beta diversity, the dissimilarity of bacteria between individuals, using principal coordinate analysis of weighted and unweighted UniFrac. Child temperament was assessed using maternal reports of the Children's Behavior Questionnaire. Finally, multiple linear regression models were tested with temperament as the response variable and alpha diversity principal components (PC) and beta diversity principal coordinates (PCo) as the explanatory variables.
Our results show that the alpha diversity PC1 had positive correlation with both weighted and unweighted Unifrac PCo1, which had positive correlation with the relative abundance of bacterial genera Ruminococcus, Alistipes, Oscillibacter, and Colidextribacter spp. and negative correlation with Veillonella, Enterococcus, Streptococcus, Escherichia, and Shigella spp. (Thus, Unifrac PCo1 was excluded from the variables of the regression model). Regression analysis revealed a significant positive association between alpha diversity PC1 and impulsivity in the Surgency/Extraversion dimension. Unweighted Unifrac PCo2 had significant positive associations with Surgency/Extraversion and impulsivity and a negative association with Negative Affectivity and some subscales linked to Negative Affectivity, such as fear (for the details, see Table 1). Unweighted Unifrac PCo2 had a positive correlation with the relative abundance of Haemophilus, Faecalibacterium, Erysipelotrichaceae, and Collinsella spp. and a negative correlation with the abundance of Eisenbergiella, Coprobacillus, and Flavonifractor spp.
We found a group of bacteria associated with alpha diversity in Japanese children. We also unraveled that alpha diversity is associated with impulsivity. It is known that Veillonella and Enterococcus spp. are the most abundant in infant gut at around 4 months of age and tend to decrease gradually with age. It was seen that if such developmental transitions are slow, the gut might be relatively premature and children tend to be less impulsive at approximately 3–5 years of age. Furthermore, we identified a group of bacteria associated with emotional expression tendencies. It was observed that the absence of Faecalibacterium, a butyric acid-producing bacterium that is abundant in adults, might be associated with high negative and low positive emotional expression. This study contributes to the further understanding of the biological mechanisms of temperament and supports the identification of predictive markers of mental health issues in later life of an individual.