Interbacterial Adhesion Networks within Early Oral Biofilms of Single Human Hosts.
Specific interbacterial adhesion, termed coaggregation, is well established for three early colonizers of the plaque biofilm: streptococci, actinomyces, and veillonellae. However, little is known about interactions of other early colonizers and about the extent of interactions within the bacterial community from a single host. To address these gaps, subject-specific culture collections from two individuals were established using an intraoral biofilm retrieval device. Molecular taxonomy (Human Oral Microbe Identification Microarray [HOMIM]) analysis of biofilm samples confirmed the integrity and completeness of the collections. HOMIM analysis verified the isolation ofStreptococcus gordoniiandS. anginosusfrom only one subject, as well as isolation of a previously uncultivated streptococcal phylotype from the other subject. Strains representative of clonal diversity within each collection were further characterized. Greater than 70% of these streptococcal strains from each subject coaggregated with at least one other coisolate. One-third of the strains carry a known coaggregation mediator: receptor polysaccharide (RPS). Almost all nonstreptococcal isolates coaggregated with other coisolates. Importantly, certainRothiastrains demonstrated more coaggregations with their coisolated bacteria than did anyStreptococcusorActinomycesstrain, and certainHaemophilusisolates participated in twice as many. Confocal microscopy of undisturbed biofilms showed thatRothiaandHaemophiluseach occur in small multispecies microcolonies. However, in confluent high-biomass regions,Rothiaoccurred in islands whereasHaemophiluswas distributed throughout. Together, the data demonstrate that coaggregation networks within an individual's oral microflora are extensive and thatRothiaandHaemophiluscan be important initiators of cell-cell interactions in the early biofilm.IMPORTANCEExtensive involvement of specific interbacterial adhesion in dental plaque biofilm formation has been postulated based onin vitrocoaggregation between oral bacteria from culture collections that are not subject specific. In the present study, subject-specific culture collections were obtained from early plaque biofilm of two volunteers, and coaggregations within each culture collection were assayed. Coaggregations, several of which involved a coaggregation-mediating cell surface molecule known from well-studied streptococci, were widespread. Unexpectedly, the little-studied organismsHaemophilusandRothiaparticipated in the greatest numbers of interactions with community members; these two organisms showed different distributions within the undisturbed biofilm. The data show that coaggregation networks encompass most organisms within the biofilm community of each individual, and they indicate prominent participation of organisms such asHaemophilusandRothiain early plaque biofilm formation.
National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland, USA rjpalmer@nih.gov.
Robert J
RJ
Palmer
National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland, USA.
Nehal
N
Shah
Eunice Kennedy Shriver National Center for Child Health and Development, National Institutes of Health, Bethesda, Maryland, USA.
Alex
A
Valm
Forsyth Institute, Cambridge, Massachusetts, USA, and Harvard School of Dental Medicine, Boston, Massachusetts, USA.
Bruce
B
Paster
Forsyth Institute, Cambridge, Massachusetts, USA, and Harvard School of Dental Medicine, Boston, Massachusetts, USA.
Floyd
F
Dewhirst
Wrigley, Chicago, Illinois, USA.
Taichi
T
Inui
National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland, USA.
John O
JO
Cisar
D000328:Adult; D001419:Bacteria / Q000145:classification / Q000235:genetics / Q000302:isolation & purification*; D001422:Bacterial Adhesion; D018407:Bacterial Physiological Phenomena; D018441:Biofilms; D003773:Dental Plaque / Q000382:microbiology*; D006801:Humans; D008297:Male; D008875:Middle Aged
Haemophilus; Rothia; biofilms; coaggregation; oral microbiome; streptococci