Investigating the Anna Karenina principle of the breast microbiome

The relationship between the microbiome and disease has long been a central focus of research in human microbiome. Inspired by Leo Tolstoy's dictum, the Anna Karenina Principle (AKP) offers a framework for understanding the complex dynamics of microbial communities in response to perturbations, suggesting that dysbiotic individuals exhibit greater variability/heterogeneity in their microbiome compared to healthy counterparts. While some studies have proved the alignment of microbiome responses to disease with the AKP effect, it remains uncertain whether the human breast microbiome responds similarly to breast disease. This study used beta-diversity and similarity in Hill numbers, along with shared species analysis (SSA), to explore this issue. We observed that during mastitis, changes in both the taxa richness and composition in the breast milk microbiome align with the AKP effect, while alterations in abundant taxa exhibit an anti-AKP effect. The response of breast tissue microbiome to breast cancer differs from that of milk microbiome to mastitis. Breast cancer induce anti-AKP effects in taxa richness, and non-AKP effects in common taxa and taxa composition. Overall, our findings identified different responses to breast diseases across taxa abundance in the breast microbiome. Mastitis primarily involves increasing the heterogeneity of rare taxa in the breast milk microbiome, while breast cancer associates with decreased dispersion of rare taxa in the tissue microbiome.