4.2 Development and stability of the human microbiome

The human microbiome undergoes significant changes throughout life, starting with initial colonization at birth. Factors like delivery method, feeding practices, and environmental exposures shape its development. As we grow, our microbiome becomes more diverse and stable, playing crucial roles in health and disease.

A stable microbiome is key to maintaining health, resisting perturbations, and recovering from disturbances. It supports essential functions like nutrient metabolism and immune regulation. Disruptions to microbiome stability, especially in early life, can have long-lasting effects on health and increase disease risks.

Human Microbiome Development

Initial Colonization and Early Influences

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• Mode of delivery impacts initial colonization of infant microbiome
  • Vaginal delivery transfers maternal vaginal and gut microbes
  • Cesarean delivery results in different initial microbial communities (skin and environmental microbes)
• Infant feeding practices shape early gut microbiome
  • Breastfeeding promotes beneficial bacteria (Bifidobacterium)
  • Formula feeding leads to different microbial composition (more diverse, less dominated by Bifidobacterium)
• Introduction of solid foods triggers microbiome shifts
  • Promotes development of adult-like microbial community
  • Increases diversity and abundance of bacteria that break down complex carbohydrates (Bacteroides, Clostridium)
• Environmental factors influence microbiome diversity
  • Antibiotic exposure can reduce diversity and alter composition
  • Pet ownership often increases microbial diversity (exposure to different microbes)
  • Siblings contribute to microbial exchange and increased diversity

Host Factors and Microbiome Maturation

• Host genetics contribute to microbiome development
  • Influence immune responses affecting microbial colonization
  • Impact mucus production creating specific niches for microbes
  • Affect metabolite availability for microbial growth (e.g., specific glycans in breast milk)
• Immune system maturation interacts with microbiome
  • Establishes tolerance to commensal microbes
  • Shapes microbial composition through selective pressure
  • Microbiome in turn educates the developing immune system
• Hormonal changes during puberty alter microbiome
  • Skin microbiome shifts (increase in Corynebacterium and Propionibacterium)
  • Gut microbiome composition changes (influenced by sex hormones)

Microbiome Stability and Health

Characteristics of a Stable Microbiome

• Microbiome stability maintains composition and function over time
  • Resists perturbations from external factors (diet changes, stress)
  • Recovers quickly after disturbances
• Core set of microbial species persist
  • Dominant species remain relatively constant (Bacteroides, Faecalibacterium)
  • Allow for fluctuations in less abundant species
• Ecological concepts applied to microbiome stability
  • Resilience describes ability to return to stable state after disturbance
  • Resistance refers to ability to withstand changes during perturbations
• Keystone species play crucial role in stability
  • Disproportionately large impact on community function (Faecalibacterium prausnitzii in gut)
  • Loss of keystone species can lead to significant community shifts

Importance of Microbiome Stability for Health

• Stable microbiome maintains physiological functions
  • Nutrient metabolism (breakdown of complex carbohydrates)
  • Immune system regulation (production of short-chain fatty acids)
  • Protection against pathogens (competitive exclusion)
• Dysbiosis associated with health conditions
  • Inflammatory bowel disease (reduced diversity, altered composition)
  • Obesity (increased Firmicutes to Bacteroidetes ratio)
  • Autoimmune disorders (loss of beneficial microbes)
• Factors promoting microbiome stability
  • Dietary fiber intake supports growth of beneficial bacteria
  • Regular exercise improves microbial diversity
  • Minimizing unnecessary antibiotic use preserves community structure

Stages of Microbiome Development

Early Life Stages

• Prenatal period involves initial microbial exposure
  • Placenta and amniotic fluid contain low levels of microbes
  • Challenges traditional view of sterile in utero environment
• Birth represents critical colonization event
  • Vaginal delivery exposes infant to maternal vaginal and gut microbes
  • Cesarean delivery results in exposure to skin and environmental microbes
• Neonatal period (0-28 days) characterized by rapid colonization
  • High instability and susceptibility to environmental influences
  • Dominated by facultative anaerobes (Escherichia coli, Enterococcus)
• Infancy (1 month to 2 years) establishes diverse microbiome
  • Strongly influenced by feeding practices (breast milk vs. formula)
  • Introduction of solid foods promotes microbial diversification

Later Stages and Adulthood

• Childhood (2-12 years) involves further diversification
  • Environmental exposures shape microbiome (school, playgrounds)
  • Lifestyle factors impact composition (diet, physical activity)
• Adolescence marked by hormonal influences on microbiome
  • Skin microbiome shifts (increase in acne-associated bacteria)
  • Gut microbiome affected by sex hormones
• Adulthood features relatively stable microbiome
  • Core microbial community established
  • Significant life events can induce shifts (pregnancy, major dietary changes)
• Elderly microbiome shows reduced diversity and stability
  • Influenced by changes in diet (reduced variety)
  • Medication use affects microbial composition (especially antibiotics)
  • Declining immune function alters host-microbe interactions

Disruptions to Microbiome Stability

Early Life Disruptions and Consequences

• Early-life antibiotic exposure alters microbiome long-term
  • Reduces diversity and alters composition
  • Increases risk of allergies, asthma, and obesity in later life
• Cesarean section delivery delays beneficial bacterial colonization
  • Lower abundance of Bifidobacterium and Bacteroides
  • Potentially contributes to increased risk of immune-mediated diseases
• Disrupted oral tolerance establishment affects immune development
  • May increase susceptibility to food allergies (peanut, egg)
  • Linked to higher risk of autoimmune disorders (celiac disease, type 1 diabetes)
• Perturbations in gut-brain axis linked to neurological issues
  • Altered microbiome composition associated with autism spectrum disorders
  • Dysbiosis implicated in depression and anxiety disorders

Adult and Elderly Microbiome Disruptions

• Chronic dysbiosis in adulthood affects metabolic function
  • Contributes to metabolic syndrome (insulin resistance, obesity)
  • Alters production of microbial metabolites (short-chain fatty acids)
• Microbiome changes in elderly exacerbate immunosenescence
  • Reduced diversity increases susceptibility to infections (Clostridium difficile)
  • May contribute to age-related diseases (Alzheimer's, Parkinson's)
• Skin microbiome disruptions lead to dermatological conditions
  • Atopic dermatitis associated with increased Staphylococcus aureus
  • Acne linked to overgrowth of Propionibacterium acnes
• Antibiotic overuse promotes antibiotic-resistant bacteria
  • Emergence of resistant strains within microbiome (MRSA, VRE)
  • Reduces overall microbial diversity and function