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Section 5
Infectious andSystemic Diseases
293
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18
Human Microbiome inHealth andDisease withReference
toDysbiosis inDental Caries andPeriodontal Diseases
Preethi Balan 1, Nadeeka Udawatte 2 and Chaminda Jayampath Seneviratne
1
Singapore Oral Microbiomics Initiative, National Dental Research Institute Singapore, National Dental Center, Singapore
2
COR3 Research Group, School of Dentistry, The University of Queensland, Brisbane, Australia
2
18.1 Introduction toHuman Microbiome
The term microbiome was defined by Joshua Lederberg in 2003 as ‘the ecological community of
commensal, symbiotic, and pathogenic microorganisms that share our body space and have been
all but ignored as determinants of health and disease’[1]. Since then, over the last two decades
(2003–2023), many publications have described the role of the human microbiome in health and
disease. Although the term microbiome was coined in 2003, the interest of community- wide effect
of oral microorganisms has a long history, especially with relevant to common oral diseases such
as dental caries and periodontal disease. The microbial aetiology of these two diseases has been
known at least since the 19th century with the general appreciation of germ theory. Hence, it will
be interesting to examine how our understanding of the role of oral microorganisms with reference to dental caries and periodontal disease has evolved over time. In this book chapter, we will
especially be focused on the last two decades, in which much new research on oral microbiomes
has emerged.
An important milestone in deciphering the human microbiome was the US National Institutes
of Health (NIH) Human Microbiome Project (HMP) launched in 2007[2]. The goal of this project
was to characterise the microbial communities found in and on the human body and their roles in
human health and disease. The HMP involved large- scale sequencing of microbial genomes and
metagenomes from various body sites, such as the gut, oral cavity, skin and urogenital tract, from
200 healthy volunteers and the development of computational and analytical tools to analyse and
interpret the data. The oral cavity has the second largest and most diverse microbiota after the gut.
Hence, in the recent years, there has been interest in research focusing on its roles in health and
disease[3]. Several oral cavity samples were collected in the HMP project, including saliva, dental
plaque and mucosal swabs from various areas like the tongue, buccal mucosa and gums. These
samples were analysed using various techniques such as 16S ribosomal RNA gene amplicon
sequencing and metagenomics to identify and quantify the microbial communities present in the
oral samples. The sequences derived from HMP oral samples provided insights into the composition and function of the oral microbiome and its potential role in oral and systemic health. The first
295
Pathological Basis of Oral and Maxillofacial Diseases, First Edition. Edited by S. R. Prabhu, Syed Ali Khurram,
OmarKujan and Merva Soluk Tekkesin.
© 2025 John Wiley & Sons Ltd. Published 2025 by John Wiley & Sons Ltd.
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296
publication of the Human Microbiome Project (HMP) ‘Structure, function and diversity of the
healthy human microbiome.’ was published in Nature in 2012[4].
18.2 Understanding theTerminology Used
inMicrobiome Research
The problem with scientific terminology is that the meaning can vary greatly based on an individual’s knowledge and understanding of the topic. This is particularly important for clinicians
who may not be familiar with new scientific terms. Hence, we advocate readers to peruse the terms
in Table18.1 that are frequently employed in oral microbiome research publications and are presented in accessible language for a lay audience. (Table18.1).
Table18.1 Terminologies used inmicrobiome research.
Term Definition
Biofilm Complex community of microbes attached to a surface or to each other, encased
Microbiome The totality of microbes, their genetic information and the environment where
Microbiota All the microbial organisms that integrate the microbiome (2)
Symbiosis A long- term relationship wherein two or more species reside in close proximity to
Dysbiosis A condition in which the balanced state of the ecosystem is disturbed. Such
Ecological balance Dynamic equilibrium and harmonious coexistence of organisms and their
Intrinsic host factors Inherent biological characteristics of the host that are in general not intentionally
Extrinsic host
factors
Homeostasis Dynamic equilibrium of a biological system understood as its ability to maintain
Internal Transcribed
Spacer (ITS)
16S rRNA gene The gene is widely present and extremely conserved across bacteria and archaea.
Hypervariable
regions of 16S rRNA
gene
Sanger sequencing The DNA sequencing technique that utilises electrophoresis and relies on the
in a self- produced extracellular polymeric matrix (1)
they interact (2)
one another (3)
disruptions are frequently associated with external factors, such as the presence
of diseases or the usage of medications (2)
environment (4)
modulated by the host (5)
Characteristics of the host that are the result of intentional modulation based on
external stimuli (5)
its essential variables constant through the mutual interaction of its components
(6)
The DNA region has been extensively sequenced in the field of molecular ecology
of fungi and is commonly regarded as the universal fungal barcode sequence.
Its absence would render bacteria/archaea incapable of translating mRNA into
functional proteins, ultimately leading to their dysfunction.
The 16S rRNA gene comprises nine hypervariable regions (V1–V9) which exhibit
variations distinguishing bacterial species and genera.
random integration of chain- terminating dideoxynucleotides by DNA polymerase
during invitro DNA replication. It enables the sequencing of individual DNA
fragments one at a time.
t.me/Dr_Mouayyad_AlbtousH
Table18.1 (Continued)
Term Definition
297
Next- Generation
Sequencing (NGS)
The sequencing technique involves fragmenting DNA/RNA into multiple
pieces, adding adapters, sequencing the libraries, and reassembling them to form
a genomic sequence. The technology is used to determine the order of nucleotides
in entire genomes or targeted regions of DNA or RNA. It sequences millions of
fragments simultaneously per run.
Full length 16S
rRNA gene
The sequencing technique aims to both species and strain resolution in
microbiota communities
sequencing
Amplicon/Targeted
gene sequencing
The common sequencing methods used to identify and compare bacteria or fungi
present within a given sample.
(16S/ITS)
Metagenomic
sequencing
The sequencing technique aims to sample all genes from a community and can
produce detailed metabolic and functional profiles. This method that allows the
identification and characterisation of organisms from all kinds of
samples (7).
Pyrosequencing The DNA sequencing technique differs from Sanger sequencing by employing
pyrophosphate release detection and light generation upon nucleotide
incorporation, instead of terminating the DNA chain with dideoxynucleotides. It
enables the identification of the genetic code within a specific segment of DNA.
Exon/Exome Each protein- coding segment of a gene is called an exon, and in combination, all
exons within the genome are known as the exome.
Whole- exome
sequencing (WES)
The sequencing technique allows variations in identification of variations within
the protein- coding region of any gene, rather than limiting the analysis to a
specific set of genes. Because most known mutations that cause disease occur in
exons, whole- exome sequencing is considered a highly effective approach for
detecting potential disease- causing mutations.
Whole- genome
sequencing (WGS)
The sequencing technique is capable of identifying all the nucleotides present in
an individual’s DNA, enabling the detection of variations across the entire
genome. Particularly valuable for identification of genetic disorders–variations
caused by DNA variations outside the exons can affect gene activity and protein
production that WGS miss.
Total RNA
sequencing
This process capturing all RNA present in the sample, including non- coding
RNAs and alternative splicing variants.
Transcriptome The complete set of transcribed genes (mRNAs) and other non- coding RNAs.
mRNA sequencing/
Transcriptome
This process specifically focusses on protein- coding transcripts, providing
superior data on the coding regions of genes.
sequencing
Metatranscriptomics The study of the function of an entire set of transcripts by RNA- sequencing from
environmental samples at a specific time.
Metatranscriptomic
sequencing
The whole expression profile by randomly sequencing mRNAs which allows for
the monitoring of gene expression patterns in microbial communities over time
using NGS
Metabolomics The study of metabolites, the chemical substances produced as a result of
metabolism, which encompasses the entirety of chemical reactions occurring
within cells to generate energy for essential biological processes.
Proteomics The study of the entire set of proteins produced by the cell.
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(Continued )
298
Table18.1 (Continued)
Term Definition
Taxonomy It is a classification of microorganisms’ systematics; in ascending order, each
Operational
taxonomic units
(OTUs)
ASV/ zero- radius
OTUs (ZOTUs)
Species richness/
Alpha diversity
Beta diversity What is the degree of species variation between different ecosystems/different
Species diversity How do the species maintain equilibrium among themselves. Is there any even
species belongs to a genus, family, class, phylum/division and domain.
Taxonomic profiling involves assigning the sequence reads to representative
sequences, known as OTUs. Typically, a sequence similarity of over 97% (or a
dissimilarity of up to 3%) is used to define a species within an OTU. For defining
genus and phylum, sequence similarities of 95 and 80% respectively are
employed. This method is applied to analyse gene sequence data sets of bacteria
and fungi, obtained through advanced sequencing technologies like metagenomic
sequencing and targeted next- generation sequencing.
A method of clustering sequences aims to identify variations in sequences, even
those caused by a single nucleotide change. This approach eliminates the need for
similarity- based clustering units, known as zero- radius OTUs. Therefore, ASVs
enabling a slightly stronger detection of fungal and bacterial diversity.
The number of different species could be detected in a microbial ecosystem/one
sample
samples
distribution of species, with similar level of abundance, or do certain species
exert dominance over others?
18.3 Oral Microbiome Associated withDental Caries
Dental caries is the most prevalent of all 291medical conditions evaluated in the Global Burden of
Disease Study worldwide[5, 6]. It affects approximately 3.1 billion people (44%), placing a major
healthcare burden globally. It is important to note that dental caries is the most common chronic
disease among children[7]. 520million children suffer from caries of primary teeth or early childhood caries (ECC), which is a fivefold higher prevalence than asthma in children[8].
18.3.1 Dental Plaque Biofilm inDental Caries
In the long- standing traditional view, the aetiology of dental caries involves four main factors: a
tooth, pathogenic microorganisms residing in dental plaque, food for pathogens or fermentable
carbohydrates, and time. Although, over time, many more factors have been recognised as contributing to the etiopathology of dental caries, the foundation of these four factors cannot be denied.
Today, we know that dental caries is indeed a multifactorial disease. Numerous factors, including
but not limited to genetics, microbial, environmental, physiological and behavioural factors, contribute to the initiation and development of dental caries[9].
As mentioned above, dental plaque is at the centre of the pathogenesis of dental caries[10, 11].
It is important to understand the difference between dental plaque biofilm and the dental plaque
microbiome[12]. In general, a biofilm is a surface- attached microbial community encased in a
matrix of exopolymeric substances. Dental plaque is attached to tooth substance and composed of
exopolymers such as glucans secreted by bacteria[10]. Hence, a biofilm essentially denotes a structural arrangement of microorganisms in which microorganisms are a part of the larger microbial
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city. In contrast, a microbiome is essentially a microbial community with its genetic material, irrespective of whether they are organised as a biofilm or not.
Based on mathematical modelling, it is estimated that the human body consists of a significantly greater quantity of microbial cells (ranging from two to three orders of magnitude) compared to eukaryotic and archaea cells[13]. In the human body, all the surface exposed to exterior
is colonised by microorganisms. This includes oral cavity, gut, skin, genitalia as well as cornea
of the eye. Oral cavity is replete with hundreds of thousands of microorganisms including various species of bacteria, fungi, viruses and protozoans. In the oral cavity, indigenous species can
access all surfaces through saliva flow, but successful adhesion and colonisation depend on
specific environmental conditions[14]. As a result, depending on the niche, whether it is on a
hard surface or a soft surface, composition of the oral microorganisms may vary. For example, a
distinctive, multi- genus consortium in the microbiome of supragingival dental plaque was
observed using spectral imaging fluorescence in situ hybridisation as guided by metagenomic
sequence analysis [15]. The microbial consortium is composed of a radially arranged, ninetaxon structure organised around cells of filamentous corynebacteria. Classical models of dental plaque biofilm highlight the critical role of Fusobacterium species in physically bridging
early and late colonisers. In contrast, this study suggested a central role of Corynebacterium as
the taxon that plays a central role by physically connecting each of the other taxa in the hedgehog structure[15].
In health, resident oral microorganisms all live in harmony or symbiosis. However, under certain conditions, often due to changes in environmental factors such as frequent intake of dietary
sugars, microbial composition may dramatically change, leading to dysbiosis of the oral microbiome. Microorganisms associated with dental caries produce acids such as lactic, formic, acetic and
propionic acids through carbohydrate metabolism. These acids lead to a decrease in pH levels
below 5.5, causing demineralisation of enamel hydroxyapatite crystals and the proteolytic breakdown of the structure of tooth hard tissues. Hence, dental caries is defined as ‘biofilm- mediated
dysbiosis that involves changes in the microbiome composition and function, which leads to the
dissolution of tooth substance (enamel and dentin) by acid produced by select oral bacteria, as a
result of the fermentation of dietary carbohydrates’[8].
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18.3.2 Microbial Models Associated withDental Caries
W. D. Miller, regarded as the first oral microbiologist, published his landmark work, ‘The
Microorganisms of the Human Mouth’, in 1891, proposing the ‘chemico- parasitic’ theory to
describe dental caries[16]. However, it was not until J. Clarke identified Streptococcus mutans in
1924 that there was confirmation of microbial pathogens associated with dental caries [17].
Through their studies, Keyes and Fitzgerald demonstrated that carries an infectious and transmissible disease[18]. Hence, in early 20th century, in line with specific- plaque hypothesis, S. mutans
has been rationalised as the major bacterial pathogen associated with dental caries. Later more
broadly, Mutans group of Streptococci, including S. mutans and Streptococcus sobrinus were
regarded as classical cariogenic pathogens. Philip Marsh proposed the ecological plaque hypothesis in 1994, combining the concept of a shift in the microbial component in dental plaque due to
environmental catastrophes, such as frequent consumption of sugar[19].
Clinical studies have observed that the caries development stage does not necessarily involve
these classical cariogenic pathogens. Therefore, Takahashi and Nyvad proposed an extended ecological plaque hypothesis that includes several other species in the overall cariogenic process[20].
The hypothesis described dental plaque as a dynamic microbial community where non- mutans
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