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<p>Periodontal diseases, including gingivitis and periodontitis, affect over a billion people globally, posing a major public health challenge due to their impact on tooth loss, systemic health, and quality of life. Traditionally, research has focused on the microbial composition of dental biofilms. However, this review highlights the critical yet underexplored role of the spatial organization or biogeography of the periodontal microbiome in disease pathogenesis. We examine biofilm development stages, focusing on molecular adhesion mechanisms and the extracellular matrix’s role in maintaining structural and microenvironmental complexity. Specific spatial architectures in periodontal biofilms such as vertical/horizontal stratification and niche formation driven by gradients in oxygen, pH, and nutrients, are discussed, alongside the spatial influence of keystone pathogens like <i>Porphyromonas gingivalis</i> and bridging organisms like <i>Fusobacterium nucleatum</i>. We also consider how microbial arrangement near host tissues influences immune evasion, barrier disruption, and cytokine responses. Advanced imaging and analytical tools, including FISH, CLSM, computational modeling, and spatial omics, are reviewed for their ability to map these dynamics. Finally, we explore the therapeutic potential of spatially-targeted strategies like disrupting microbial interactions, targeting niches, and enabling personalized interventions based on spatial profiling. Integrating spatial microbiology with systems biology and immunology offers a promising framework for advancing periodontal disease understanding and treatment.</p> Graphical abstract <p></p>

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A comprehensive review of microbial spatial organization in periodontal pathogenesis

  • 期刊论文

  • 发表日期：

    2025年6月26日

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  • Basavaraj Neelappa Gonal,
  • Nagarjuna Prakash Dalbanjan,
  • Arihant Jayawant Kadapure,
  • Maruti J. Gurav,
  • Vishwanath B. Chachadi,
  • S. K. Praveen Kumar,
  • Suresh B. Arakera

摘要

Periodontal diseases, including gingivitis and periodontitis, affect over a billion people globally, posing a major public health challenge due to their impact on tooth loss, systemic health, and quality of life. Traditionally, research has focused on the microbial composition of dental biofilms. However, this review highlights the critical yet underexplored role of the spatial organization or biogeography of the periodontal microbiome in disease pathogenesis. We examine biofilm development stages, focusing on molecular adhesion mechanisms and the extracellular matrix’s role in maintaining structural and microenvironmental complexity. Specific spatial architectures in periodontal biofilms such as vertical/horizontal stratification and niche formation driven by gradients in oxygen, pH, and nutrients, are discussed, alongside the spatial influence of keystone pathogens like Porphyromonas gingivalis and bridging organisms like Fusobacterium nucleatum. We also consider how microbial arrangement near host tissues influences immune evasion, barrier disruption, and cytokine responses. Advanced imaging and analytical tools, including FISH, CLSM, computational modeling, and spatial omics, are reviewed for their ability to map these dynamics. Finally, we explore the therapeutic potential of spatially-targeted strategies like disrupting microbial interactions, targeting niches, and enabling personalized interventions based on spatial profiling. Integrating spatial microbiology with systems biology and immunology offers a promising framework for advancing periodontal disease understanding and treatment.

Graphical abstract