Polymicrobial Aggregates in Human Saliva Build the Oral Biofilm
Por:
Simon-Soro A, Ren Z, Krom BP, Hoogenkamp MA, Cabello-Yeves PJ, Daniel SG, Bittinger K, Tomas I, Koo H and Mira A
Publicada:
1 ene 2022
Ahead of Print:
22 feb 2022
Resumen:
Biofilm community development has been established as a sequential process starting from the attachment of single cells on a surface. However, microorganisms are often found as aggregates in the environment and in biological fluids. Here, we conduct a comprehensive analysis of the native structure and composition of aggregated microbial assemblages in human saliva and investigate their spatiotemporal attachment and biofilm community development. Using multiscale imaging, cell sorting, and computational approaches combined with sequencing analysis, a diverse mixture of aggregates varying in size, structure, and microbial composition, including bacteria associated with host epithelial cells, can be found in saliva in addition to a few single-cell forms. Phylogenetic analysis reveals a mixture of complex consortia of aerobes and anaerobes in which bacteria traditionally considered early and late colonizers are found mixed together. When individually tracked during colonization and biofilm initiation, aggregates rapidly proliferate and expand tridimensionally, modulating population growth, spatial organization, and community scaffolding. In contrast, most single cells remain static or are incorporated by actively growing aggregates. These results suggest an alternative biofilm development process whereby aggregates containing different species or associated with human cells collectively adhere to the surface as "growth nuclei" to build the biofilm and shape polymicrobial communities at various spatial and taxonomic scales.
IMPORTANCE Microbes in biological fluids can be found as aggregates. How these multicellular structures bind to surfaces and initiate the biofilm life cycle remains understudied. Here, we investigate the structural organization of microbial aggregates in human saliva and their role in biofilm formation. We found diverse mixtures of aggregates with different sizes, structures, and compositions in addition to free-living cells. When individually tracked during binding and growth on tooth-like surfaces, most aggregates developed into structured biofilm communities, whereas most single cells remained static or were engulfed by the growing aggregates. Our results reveal that preformed microbial consortia adhere as "buds of growth," governing biofilm initiation without specific taxonomic order or cell-by-cell succession, which provide new insights into spatial and population heterogeneity development in complex ecosystems.
Filiaciones:
Simon-Soro A:
Biofilm Research Laboratories, Department of Orthodontics, Divisions of Community Oral Health & Pediatric Dentistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Center for Advanced Research in Public Health, FISABIO Foundation, Valencia, Spain
Ren Z:
Biofilm Research Laboratories, Department of Orthodontics, Divisions of Community Oral Health & Pediatric Dentistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Krom BP:
Department of Preventive Dentistry, Academic Centre for Dentistry Amsterdam, University of Amsterdam and Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Hoogenkamp MA:
Department of Preventive Dentistry, Academic Centre for Dentistry Amsterdam, University of Amsterdam and Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Cabello-Yeves PJ:
Center for Advanced Research in Public Health, FISABIO Foundation, Valencia, Spain
Daniel SG:
Division of Gastroenterology, Hepatology, and Nutrition, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA
Bittinger K:
Division of Gastroenterology, Hepatology, and Nutrition, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA
Tomas I:
Oral Sciences Research Group, Special Needs Unit, Department of Surgery and Medical-Surgical Specialties, School of Medicine and Dentistry, Universidade de Santiago de Compostela, Health Research Institute Foundation of Santiago (FIDIS), Santiago de Compostela, Spain
Koo H:
Biofilm Research Laboratories, Department of Orthodontics, Divisions of Community Oral Health & Pediatric Dentistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Center for Innovation & Precision Dentistry, School of Dental Medicine and School of Engineering & Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, USA
:
Center for Advanced Research in Public Health, FISABIO Foundation, Valencia, Spain
CIBER Center for Epidemiology and Public Health, Madrid, Spain
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