The social structure of microbial community involved in colonization resistance

Abstract

It is well established that host-associated microbial communities can interfere with the colonization and establishment of microbes of foreign origins, a phenomenon often referred to as bacterial interference or colonization resistance. However, due to the complexity of the indigenous microbiota, it has been extremely difficult to elucidate the community colonization resistance mechanisms and identify the bacterial species involved. In a recent study, we have established an in vitro mice oral microbial community (O-mix) and demonstrated its colonization resistance against an Escherichia coli strain of mice gut origin. In this study, we further analyzed the community structure of the O-mix by using a dilution/regrowth approach and identified the bacterial species involved in colonization resistance against E. coli. Our results revealed that, within the O-mix there were three different types of bacterial species forming unique social structure. They act as 'Sensor', 'Mediator' and 'Killer', respectively, and have coordinated roles in initiating the antagonistic action and preventing the integration of E. coli. The functional role of each identified bacterial species was further confirmed by E. coli-specific responsiveness of the synthetic communities composed of different combination of the identified players. The study reveals for the first time the sophisticated structural and functional organization of a colonization resistance pathway within a microbial community. Furthermore, our results emphasize the importance of 'Facilitation' or positive interactions in the development of community-level functions, such as colonization resistance.

What Are We Learning and What Can We Learn from the Human Oral Microbiome Project?

“…Fecal transplantation has been shown to effectively alter the microbiome of the gut [72, 73], but this method would be very difficult to implement in the oral cavity. The salivary flow and normal use of the mouth complicate the delivery of the new microbiome, and pre-established biofilms on enamel surfaces inhibit colonization by new species and are difficult to remove [69, 74]. Bacteriocins, antibiotic peptides produced by bacteria, are a potential new class of narrow-spectrum antibiotics [75, 76].…”

“…al. [74] identified a specific “social structure” of three species from the mouse oral microbiome that synergistically cooperate to inhibit the colonization by Escherichia coli . Staphylococcus saprophyticus senses the E. coli LPS and produces a diffusible signal that directly increases peroxide production by Streptococcus sanguinis .…”

Dynamics of an experimental microbial invasion

“…Indeed, few available experimental studies of microbial invasions have been designed to directly test such hypotheses, but, interestingly, they tend to suggest that interspecific interactions, rather than diversity per se, play critical roles in invasion resistance (14)(15)(16), although nutrient supply (17) and propagule pressure (18) have also been shown to facilitate microbial invasions.…”

Comparison of genes required for H2O2 resistance in Streptococcus gordonii and Streptococcus sanguinis

“…As initial colonizers of the saliva coated toothsurface, they promote the successive integration of several bacterial species into the developing oral biofilm by providing specific surface receptors for later colonizers (Kolenbrander et al, 2006;Rosan & Lamont, 2000). Under healthy conditions, this would lead to a benign biofilm community able to provide protection against invading species and keep opportunistic pathogens like Streptococcus mutans in low abundance (Brook, 1999;He et al, 2014;Reid et al, 2001). …”