Mini-review Microbial Coaggregation Ubiquity and Implications for Biofilm Development

Journal home page for Journal of Molecular Biology

Abstract

The oral cavity is accessible to microorganisms, and biofilms are present throughout on hard and soft tissues. The shedding of epithelial cell layers is usually constructive for controlling biofilm evolution on soft tissues. Innate immune mechanisms are not so effective confronting biofilms on molar surfaces, and oral hygiene measures such as brushing and flossing are required for the periodic removal of dental plaque. Even with good oral hygiene, microbial communities accrue on teeth in areas that are protected from mechanical abrasion forces. Changes in the composition of these biofilms are associated with oral diseases such as dental caries or periodontitis. Newly formed biofilms and more than mature dental plaque each have a level of spatial organisation in the horizontal and vertical planes. Communities are shaped by many varied interactions between dissimilar species and genera within the biofilm, which include physical cell–cell associations known as coaggregation, interspecies signaling, secretion and turnover of antimicrobial compounds and the sharing of an extracellular matrix. Key to these interactions is the choice for metabolic synergies and it is becoming clear that the ability of communities to extract the maximum energy from the available metabolites is a potent driver for biofilm structure and stratification. This review discusses recent advances in our understanding of intermicrobial interactions in oral biofilms and the roles that they play in determining the spatial organization of biofilm communities.

Introduction

Biofilms form on all exposed surfaces throughout the mouth including soft tissues and artificial materials such as implants or dentures. However, it is the biofilms on teeth, known as dental plaque, that are largely responsible for the nearly common oral diseases in humans, dental caries and periodontitis. Despite major advances in oral health over the final few decades, including significant reductions in levels of dental caries in developed countries, both caries and periodontitis remain highly prevalent in populations worldwide [1]. In the United Kingdom, for case, a recent survey plant that 46% of children aged 15 years had obvious disuse feel in their permanent teeth [ii]. Approximately 45% of adults in the United Kingdom accept moderate to avant-garde periodontitis, an irreversible status that involves loss of supporting structures effectually the teeth [3]. The architecture and limerick of dental plaque have been studied since well before the term "biofilm" was coined to depict surface-associated matrix-enclosed microbial communities in the late 1970s. Fifty-fifty so, it is only with the recent widespread introduction of "-omics" technologies that we take begun to obtain a global perspective on the compatibilities betwixt unlike microorganisms (co-occurrence relationships) and the cardinal interactions such as metabolic cooperation and competition that drive the spatial organization of microorganisms inside dental plaque. It is believed that these interactions are critical for individual organisms within dental plaque to thrive, equally well as for the community to function effectively as a whole.

The outset observations of dental plaque bacteria were fabricated by Antonie van Leeuwenhoek as far back as 1683 [iv], yet it took more 250 years before details of the structure of intact dental plaque became credible. The introduction of electron microscopy provided the offset detailed insights into the architecture of dental plaque and revealed areas where similar cell types were plain bundled in microcolonies. In addition, there was ofttimes a consistent spatial organization running through mature dental plaque from the inner layers to the outside, with Gram-positive cocci predominating at the base of dental plaque biofilms and filamentous cells more abundant in the outer layers (Fig. 1) [five], [six]. More recently, fluorescence in situ hybridization (FISH) has been applied to place taxa within these communities. Once again, this has highlighted the not-random distribution of different microorganisms within dental plaque [7], [eight]. In fact, with the utilise of combinatorial labeling and spectral imaging to extend the range of probes that could exist visualized in FISH, it was possible to visualize fifteen different taxa within a single dental plaque sample [7]. Many spatial interactions between dissimilar taxa were observed and the genera Prevotella and Actinomyces, in particular, were plant to associate with a wide range of microorganisms. Our understanding of dental plaque communities at the whole-organization level has also been greatly avant-garde by improvements in DNA sequencing and computational biology over the last decade or so, which have enabled the elevation-down characterization of circuitous microbial communities at a level of resolution well beyond anything that was previously possible. When used in combination with more traditional approaches for the detailed investigation of specific microbial interactions, these new methods hope to revolutionize our understanding of dental plaque communities.

Section snippets

The Formation and Composition of Dental Plaque

On exposed surfaces of teeth and in the presence of regular oral hygiene such equally daily toothbrushing, dental plaque undergoes a continual cycle of removal and recolonization followed by regrowth. From their first eruption in childhood, tooth surfaces are permanently covered in an acquired enamel pellicle, comprising a layer of proteins and glycoproteins that forms by selective adsorption of salivary components and is non fully removed past toothbrushing [9]. The first microorganisms to colonize

The Role of Coaggregation and Coadhesion

To colonize tooth surfaces, leaner must attach strongly to the saliva pellicle or to other cells that tin can bind to the molar. The process of cell–cell binding betwixt two genetically singled-out microorganisms is known equally coaggregation. If one cell type is already fastened to the surface, the binding is chosen coadhesion. Coaggregation between many oral microorganisms is easily detected in the laboratory by vigorously mixing full-bodied suspensions of each jail cell type and observing the formation

Exchange of Soluble Factors

Inside dental plaque, many different taxa coexist in close proximity with ane another. Each cell type utilizes different substrates from the external milieu, and each secretes different products. The changes in the external medium may then be sensed by neighboring microorganisms. A great deal of attention has been focused on identifying the cardinal extracellular factors that influence interactions between 2 or more than different microorganisms in dental plaque. Broadly, these can exist divided into

Spatial Gradients and the Part of the Extracellular Matrix

Soluble factors do not motion freely through biofilms, and many pocket-sized molecules are distributed in spatial gradients across the biofilm (Fig. 5; reviewed in Ref. [66]). Cells themselves grade a barrier to the free movement of molecules and the extracellular macromolecular matrix, which is often negatively charged, acts as an ion-substitution resin to retard the movement of charged or reactive compounds through the biofilm [67]. The matrix also slows improvidence of relatively large uncharged molecules,

Co-Occurrence Patterns in Dental Plaque Microbial Communities

Many of the techniques used for the top-down analysis of complex microbial communities, such equally Dna sequencing, RNA sequencing, proteomics and metabolomics, require extraction of molecules from the biofilm and therefore lose any data about the spatial system of cells. Nevertheless, these methods are starting to provide important insights into the outcomes of intermicrobial interactions, for example, by showing which taxa co-occur within dental plaque biofilms in health or illness.

Metabolic Models of Interspecies Interactions

Co-occurrence and co-exclusion patterns on their own do not consider biological information and therefore provide little insight into the mechanisms driving the associates of microbial communities. It is possible, however, to incorporate empirical or predictive biological data into computational models of ecosystem associates, and this can provide indications about the forces that influence the structuring of communities. So far, these models have depended largely on information about

Summary and Future Prospects

The microbial communities in oral biofilms are highly organized both spatially and temporally. In terms of the species present, in that location is a nifty bargain of consistency between different individuals. Nevertheless, there are besides important inter-individual differences that are only just first to exist understood. For example, there is evidence that people of different ethnic origin harbor distinct oral microbial communities [98]. Recently, it was shown that Halomonas hamiltonii is a predominant

References (101)

et al.
Differential consequence of autoinducer 2 of Fusobacterium nucleatum on oral streptococci

Arch. Oral Biol.

(2013)
S. Redanz et al.
Heterologous expression of sahH reveals that biofilm formation is autoinducer-2-independent in Streptococcus sanguinis simply is associated with an intact activated methionine cycle

J. Biol. Chem.

(2012)
F. Chi et al.
Crossing the bulwark: Evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, South. mitis and S. oralis

Int. J. Med. Microbiol.

(2007)
S. Messaoudi et al.
Lactobacillus salivarius: Bacteriocin and probiotic activity

Food Microbiol.

(2013)
C. Hannig et al.
Fluorescence microscopic visualization and quantification of initial bacterial colonization on enamel in situ

Arch. Oral Biol.

(2007)
S. Purushotham et al.
The calcium-induced conformation and glycosylation of scavenger-rich cysteine repeat (SRCR) domains of glycoprotein 340 influence the loftier affinity interaction with antigen I/2 homologs

J. Biol. Chem.

(2014)
1000.P. Heim et al.
Identification of a supramolecular functional architecture of Streptococcus mutans adhesin P1 on the bacterial cell surface

J. Biol. Chem.

(2015)
A.H. Nobbs et al.
Generic determinants of Streptococcus colonization and infection

Infect. Genet. Evol.

(2015)
P.E. Petersen
The World Oral Wellness Report 2003: Continuous comeback of oral health in the 21st century—The arroyo of the WHO Global Oral Health Programme

Community Dent. Oral Epidemiol.

(2003)
N. Pitts et al.
Children's Dental Health Survey 2013 Report 2: Dental Illness and Damage in Children: England

Wales and Northern Ireland

(2015)

D.A. White et al.

Adult Dental Health Survey 2009: Common oral health weather condition and their touch on on the population

Br. Dent. J.

(2012)

H. Gest

The discovery of microorganisms by Robert Hooke and Antoni Van Leeuwenhoek, fellows of the Imperial Order

Notes Rec. R. Soc. Lond.

(2004)

M.A. Listgarten

Structure of the microbial flora associated with periodontal wellness and disease in man. A light and electron microscopic study

J. Periodontol.

(1976)

H. Takeuchi et al.

Ultrastructural analysis of structural framework in dental plaque developing on synthetic carbonate apatite applied to human tooth surfaces

Eur. J. Oral Sci.

(2001)

A.M. Valm et al.

Systems-level assay of microbial community organization through combinatorial labeling and spectral imaging

Proc. Natl. Acad. Sci. U. South. A.

(2011)

V. Zijnge et al.

Oral biofilm architecture on natural teeth

PLoS One

(2010)

Y.H. Lee et al.

Proteomic evaluation of acquired enamel pellicle during in vivo formation

PLoS Ane

(2013)

A.H. Nobbs et al.

Stick to your gums: Mechanisms of oral microbial adherence

J. Dent. Res.

(2011)

L.J. Brady et al.

The changing faces of Streptococcus antigen I/II polypeptide family adhesins

Mol. Microbiol.

(2010)

P.I. Diaz et al.

Molecular label of subject-specific oral microflora during initial colonization of enamel

Appl. Environ. Microbiol.

(2006)

I. Dige et al.

Actinomyces naeslundii in initial dental biofilm formation

Microbiology

(2009)

T. Takeshita et al.

Dental plaque development on a hydroxyapatite deejay in immature adults observed by using a barcoded pyrosequencing approach

Sci. Rep.

(2015)

D. Langfeldt et al.

Composition of microbial oral biofilms during maturation in immature healthy adults

PLoS One

(2014)

J.O. Kistler et al.

Bacterial customs development in experimental gingivitis

PLoS I

(2013)

O.J. Park et al.

Pyrosequencing assay of subgingival microbiota in distinct periodontal weather

J. Dent. Res.

(2015)

A.Fifty. Griffen et al.

Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing

ISME J.

(2012)

A.C. Tanner et al.

Cultivable anaerobic microbiota of severe early childhood caries

J. Clin. Microbiol.

(2011)

G. Schulze-Schweifing et al.

Comparison of bacterial civilisation and 16S rRNA community profiling past clonal analysis and pyrosequencing for the characterization of the dentine caries-associated microbiome

Front end. Cell. Infect. Microbiol.

(2014)

T. Chen et al.

The Human Oral Microbiome Database: A Web Accessible Resource for Investigating Oral Microbe Taxonomic and Genomic Information

Database (Oxford). 2010

(2010)

A. Simón-Soro et al.

Metatranscriptomics reveals overall agile bacterial composition in caries lesions

J. Oral Microbiol.

(2014)

S. Katharios-Lanwermeyer et al.