Uncovering complex microbiome activities via metatranscriptomics during 24 hours of oral biofilm assembly and maturation
Open accessAbstract
BACKGROUND: Dental plaque is composed of hundreds of bacterial taxonomic units and represents one of the most diverse and stable microbial ecosystems associated with the human body. Taxonomic composition and functional capacity of mature plaque is gradually shaped during several stages of community assembly via processes such as co-aggregation, competition for space and resources, and by bacterially produced reactive agents. Knowledge on the dynamics of assembly within complex communities is very limited and derives mainly from studies composed of a limited number of bacterial species. To fill current knowledge gaps, we applied parallel metagenomic and metatranscriptomic analyses during assembly and maturation of an in vitro oral biofilm. This model system has previously demonstrated remarkable reproducibility in taxonomic composition across replicate samples during maturation. RESULTS: Time course analysis of the biofilm maturation was performed by parallel sampling every 2-3 h for 24 h for both DNA and RNA. Metagenomic analyses revealed that community taxonomy changed most dramatically between three and six hours of growth when pH dropped from 6.5 to 5.5. By applying comparative metatranscriptome analysis we could identify major shifts in overall community activities between six and nine hours of growth when pH dropped below 5.5, as 29,015 genes were significantly up- or down- expressed. Several of the differentially expressed genes showed unique activities for individual bacterial genomes and were associated with pyruvate and lactate metabolism, two-component signaling pathways, production of antibacterial molecules, iron sequestration, pH neutralization, protein hydrolysis, and surface attachment. Our analysis also revealed several mechanisms responsible for the niche expansion of the cariogenic pathogen Lactobacillus fermentum. CONCLUSION: It is highly regarded that acidic conditions in dental plaque cause a net loss of enamel from teeth. Here, as pH drops below 5.5 pH to 4.7, we observe blooms of cariogenic lactobacilli, and a transition point of many bacterial gene expression activities within the community. To our knowledge, this represents the first study of the assembly and maturation of a complex oral bacterial biofilm community that addresses gene level functional responses over time.
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Biofilm formation is initiated by specific primary colonizers that adhere to mucosal and dental surfaces and serve as a foundation for other bacteria through specific adhesin-receptor interactions.
“Biofilm formation is initiated by specific bacteria that are considered ‘primary colonizers’ because they adhere to mucosal and dental surfaces and serve as a foundation to which other bacteria can attach and join the community through specific adhesin-receptor interactions [1–3].”
From Coaggregation of oral pathogens by postbiotic lactobacilli (2025) · cites this paper as [1]
The Background (page unavailable) says supragingival biofilms begin with bacterial attachment to the tooth surface and identifies streptococci as common initial colonizers, followed by secondary colonizers. The Results and discussion (page unavailable) describe co-aggregating and adhesin proteins involved in a specific interaction between Fusobacterium and Streptococcus. The copy does not establish that primary colonizers adhere to mucosal surfaces or that the broader sequence of attachment occurs through specific adhesin–receptor interactions. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn the oral cavity, coaggregation plays a crucial role in the formation and stability of dental biofilm and thus influences oral health and disease.
“In the oral cavity, coaggregation plays a crucial role in the formation and stability of dental biofilm, and it thus influences oral health and disease.”
From Coaggregation of oral pathogens by postbiotic lactobacilli (2025) · cites this paper as [1]
The Results and discussion section mentions a co-aggregating protein involved in physical interactions between two oral bacterial groups. The Background links oral biofilm assembly and composition to oral health and disease, but the paper does not establish that coaggregation itself is crucial to biofilm formation or stability, or that it consequently influences health and disease. No page numbers are available in our copy. (LLM, conf=0.82)
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References 103 · Cited by 57
- Authors
- Edlund, A., Yang, Y., Yooseph, S., He, X., Shi, W., & McLean, J. S.
- Affiliations
- J. Craig Venter Institute (US)
- Marine Biodiversity Institute of Korea (KR)
- University of Central Florida (US)
- The Forsyth Institute (US)
- University of Washington (US)
- Corresponding author
- Edlund, Anna
- McLean, Jeffrey S.
- Venue
- Microbiome
- Published
- 2018-12
- Volume
- 6
- Issue
- 1
- Pages
- 217-217
- ISSN
- 2049-2618 (ISSN-L)
- PMC
- PMC6284299
- OpenAlex
- W2903048549
- Cited by
- 57
- References
- 103
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 9 · 2023: 9 · 2022: 3 · 2021: 8 · 2020: 6 · 2019: 5
- FWCI
- 5.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Microbiome (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Journal of International Crisis and Risk Communication Research (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Dental and Craniofacial Research (R00DE024543, K99DE024543, 1R01DE023810, 1R01DE020102, 1R01DE026186)
- National Institute of General Medical Sciences (R01GM095373)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- dental plaque, biofilm maturation, metatranscriptomics, metagenomics, gene expression dynamics, pH reduction, Lactobacillus fermentum, cariogenic bacteria, niche expansion, pyruvate metabolism, lactate metabolism, two-component systems, iron sequestration, pH neutralization, proteolysis, bacterial community assembly, enamel erosion
- MeSH terms
- Adult, Bacteria, Bacterial Proteins, Dental Plaque, DNA, Bacterial, DNA, Ribosomal, Humans, Hydrogen-Ion Concentration, Mouth, RNA, Ribosomal, 16S, Gene Expression Regulation, Bacterial, Sequence Analysis, DNA, Biofilms, Gene Expression Profiling, Metabolic Networks and Pathways, Metagenomics
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