Interkingdom networking within the oral microbiome

Nobbs, Angela H.; Jenkinson, Howard F.

doi:10.1016/j.micinf.2015.03.008

Cited by 50 publications

(38 citation statements)

References 70 publications

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“…Cross-kingdom coadhesion between oral streptococci and Candida albicans is also well-documented. The functionally versatile streptococcal SspA/B protein mediates this attachment through binding to the glycosylphosphatidylinositol (GPI)-linked candida cell wall protein Als3 [6]. The Als3 protein is uniquely expressed on hyphae, and hence streptococci decorate the hyphal surfaces of C. albicans in mixed-species communities.…”

Section: Linkedin: Community Infrastructurementioning

confidence: 99%

Dancing with the Stars: How Choreographed Bacterial Interactions Dictate Nososymbiocity and Give Rise to Keystone Pathogens, Accessory Pathogens, and Pathobionts

Hajishengallis

Lamont

2016

Trends in Microbiology

236

228

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Many diseases that originate on mucosal membranes ensue from the action of polymicrobial communities of indigenous organisms working in concert to disrupt homeostatic mechanisms. Multi-level physical and chemical communication systems among constituent organisms underlies polymicrobial synergy and dictates the community’s pathogenic potential or nososymbiocity, that is, disease arising from living together with a susceptible host. Functional specialization of community participants, often originating from metabolic co-dependence, has given rise to several newly appreciated designations within the commensal-to-pathogen spectrum. Accessory pathogens, while inherently commensal in a particular microenvironment, nonetheless enhance the colonization or metabolic activity of pathogens. Keystone pathogens (bacterial drivers or alpha-bugs) exert their influence at low abundance by modulating both the composition and levels of community participants and by manipulating host responses. Pathobionts (or bacterial passengers) exploit disrupted host homeostasis to flourish and promote inflammatory disease. In this review we will discuss how commensal or pathogenic properties of organisms are not intrinsic features, and have to be considered within the context of both the microbial community in which they reside and the host immune status.

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Section: Linkedin: Community Infrastructurementioning

confidence: 99%

Dancing with the Stars: How Choreographed Bacterial Interactions Dictate Nososymbiocity and Give Rise to Keystone Pathogens, Accessory Pathogens, and Pathobionts

Hajishengallis

Lamont

2016

Trends in Microbiology

236

228

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“…The bacteria that colonize this niche contend with a high density of competing bacteria of an estimated 2,000 different taxa and dramatic environmental changes that are dependent on host behavior (1,2). Streptococcus gordonii is a pioneer colonizer of this environment, where it initiates biofilm formation by binding directly to the acquired salivary pellicle on the tooth surface (2,3).…”

mentioning

confidence: 99%

Mutation of the Thiol-Disulfide Oxidoreductase SdbA Activates the CiaRH Two-Component System, Leading to Bacteriocin Expression Shutdown in Streptococcus gordonii

2016

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Streptococcus gordonii is a commensal inhabitant of the human oral cavity. To maintain its presence as a major component of oral biofilms, S. gordonii secretes inhibitory molecules such as hydrogen peroxide and bacteriocins to inhibit competitors. S. gordonii produces two nonmodified bacteriocins (i.e., Sth 1 and Sth 2 ) that are regulated by the Com two-component regulatory system, which also regulates genetic competence. Previously we found that the thiol-disulfide oxidoreductase SdbA was required for bacteriocin activity; however, the role of SdbA in Com signaling was not clear. Here we demonstrate that ⌬sdbA mutants lacked bacteriocin activity because the bacteriocin gene sthA was strongly repressed and the peptides were not secreted. Addition of synthetic competence-stimulating peptide to the medium reversed the phenotype, indicating that the Com pathway was functional but was not activated in the ⌬sdbA mutant. Repression of bacteriocin production was mediated by the CiaRH two-component system, which was strongly upregulated in the ⌬sdbA mutant, and inactivation of CiaRH restored bacteriocin production. The CiaRH-induced protease DegP was also upregulated in the ⌬sdbA mutant, although it was not required for inhibition of bacteriocin production. This establishes CiaRH as a regulator of Sth bacteriocin activity and links the CiaRH and Com systems in S. gordonii. It also suggests that either SdbA or one of its substrates is an important factor in regulating activation of the CiaRH system. IMPORTANCEStreptococcus gordonii is a noncariogenic colonizer of the human oral cavity. To be competitive in the oral biofilm, S. gordonii secretes antimicrobial peptides called bacteriocins, which inhibit closely related species. Our previous data showed that mutation of the disulfide oxidoreductase SdbA abolished bacteriocin production. In this study, we show that mutation of SdbA generates a signal that upregulates the CiaRH two-component system, which in turn downregulates a second two-component system, Com, which regulates bacteriocin expression. Our data show that these systems are also linked in S. gordonii, and the data reveal that the cell's ability to form disulfide bonds is sensed by the CiaRH system. O ral biofilms are highly competitive, constantly fluctuating environments. The bacteria that colonize this niche contend with a high density of competing bacteria of an estimated 2,000 different taxa and dramatic environmental changes that are dependent on host behavior (1, 2). Streptococcus gordonii is a pioneer colonizer of this environment, where it initiates biofilm formation by binding directly to the acquired salivary pellicle on the tooth surface (2, 3). Once established, S. gordonii persists within the host as part of the oral microbiota. The presence of S. gordonii is associated with oral health (4, 5), and it has been shown to inhibit biofilm formation by cariogenic species (6, 7).S. gordonii uses several strategies to gain advantage over its competitors and to colonize the oral cavity successfully...

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“…We are finding many more phyla than expected and there is a great deal of inter-host variability (e.g., not more, and likely less, than 30% of fecal bacteria species are shared across individuals; Faith et al 2013). Thus, determining and then understanding even a specific microbiome network of even a single region of a single individual's whole within-host ecosystem appears daunting (e.g., see Nobbs and Jenkinson 2015) which reviews the diverse players of the inter-kingdom network of the oral ecosystem). The many players include bacteria, host cells (as the physical environment and as resources), bacteriophages, yeast, fungi, viruses and, not the least, immunity cells and compounds.…”

Section: Quantitative Formulation Of a Microbiomementioning

confidence: 99%

“…Many insights, concepts and discoveries are found in very distant fields with often little communication with one another (e.g., microbiology, immunology, various clinical fields, community ecology, evolutionary biology, and invasion biology where insights are often found in the plant or conservation literature). Also, the discovery of the members of WH communities has created a picture of an inter-kingdom network, replete with bacteria, viruses, fungi and archaea (Horz 2015;Huffnagle and Noverr 2013;Lecuit and Eloit 2013;Nobbs and Jenkinson 2015). We believe that ecological and evolutionary theory can be a unifying framework from which patterns and principles can emerge.…”

mentioning

confidence: 97%

Invasions of Host-Associated Microbiome Networks

Murall

Abbate

Touzel

et al. 2017

Networks of Invasion: Empirical Evidence and Case Studies

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International audienceThe study of biological invasions of ecological systems has much to offer research on within–host (WH) systems, particularly for understanding infections and developing therapies using biological agents. Thanks to the ground-work established in other fields, such as community ecology and evolutionary biology, and to modern methods of measurement and quantification, the study of microbiomes has quickly become a field at the forefront of modern systems biology. Investigations of host-associated microbiomes (e.g. for studying human health) are often centred on measuring and explaining the structure, functions and stability of these communities. This momentum promises to rapidly advance our understanding of ecological networks and their stability, resilience and resistance to invasions. However, intrinsic properties of host-associated microbiomes that differ from those of free-living systems present challenges to the development of a WH invasion ecology framework. The elucidation of principles underlying the invasibility of WH networks will ultimately help in the development of medical applications and help shape our understanding of human health and disease

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Interkingdom networking within the oral microbiome

Cited by 50 publications

References 70 publications

Dancing with the Stars: How Choreographed Bacterial Interactions Dictate Nososymbiocity and Give Rise to Keystone Pathogens, Accessory Pathogens, and Pathobionts

Dancing with the Stars: How Choreographed Bacterial Interactions Dictate Nososymbiocity and Give Rise to Keystone Pathogens, Accessory Pathogens, and Pathobionts

Mutation of the Thiol-Disulfide Oxidoreductase SdbA Activates the CiaRH Two-Component System, Leading to Bacteriocin Expression Shutdown in Streptococcus gordonii

Invasions of Host-Associated Microbiome Networks

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