Autoinducer 2-Dependent Escherichia coli Biofilm Formation Is Enhanced in a Dual-Species Coculture.

Leanid Laganenka,Victor Sourjik,Harold L Drake

doi:10.1128/aem.02638-17

Abstract

ABSTRACTBiofilms in nature typically consist of multiple species, and microbial interactions are likely to have crucial effects on biofilm development, structure, and functions. The best-understood form of communication within bacterial communities involves the production, release, and detection of signal molecules (autoinducers), known as quorum sensing. Although autoinducers mainly promote intraspecies communication, autoinducer 2 (AI-2) is produced and detected by a variety of bacteria, thus principally allowing interspecies communication. Here we show the importance of AI-2-mediated signaling in the formation of mixed biofilms by Enterococcus faecalis and Escherichia coli. Our results demonstrate that AI-2 produced by E. faecalis promotes collective behaviors of E. coli at lower cell densities, enhancing autoaggregation of E. coli but also leading to chemotaxis-dependent coaggregation between the two species. Finally, we show that formation of such mixed dual-species biofilms increases the stress resistance of both E. coli and E. faecalis.IMPORTANCE The role of interspecies communication in the development of mixed microbial communities is becoming increasingly apparent, but specific examples of such communication remain limited. The universal signal molecule AI-2 is well known to regulate cell-density-dependent phenotypes of many bacterial species but, despite its potential for interspecies communication, the role of AI-2 in the establishment of multispecies communities is not well understood. In this study, we explore AI-2 signaling in a dual-species community containing two bacterial species that naturally cooccur in their mammalian hosts, i.e., Escherichia coli and Enterococcus faecalis. We show that active production of AI-2 by E. faecalis allows E. coli to perform collective behaviors at low cell densities. Additionally, AI-2- and chemotaxis-dependent coaggregation with E. faecalis creates nucleation zones for rapid growth of E. coli microcolonies in mixed biofilms and enhances the stress resistance of both species.

Highlights

Biofilms in nature typically consist of multiple species, and microbial interactions are likely to have crucial effects on biofilm development, structure, and functions
We observed that E. coli biofilms formed under these conditions were apparently more structured when grown in cocultures with E. faecalis (Fig. 2A and B; see Fig. S1A in the supplemental material)
Microcolonies formed by E. coli and E. faecalis apparently colocalized within these mixed biofilms (Fig. 2B and C)

Summary

Introduction

Biofilms in nature typically consist of multiple species, and microbial interactions are likely to have crucial effects on biofilm development, structure, and functions. QS is based on production of, secretion of, and subsequent concentration-dependent responses to signal molecules (autoinducers) This process plays a role in various types of collective bacterial behaviors, including biofilm formation and colonization of plant and animal hosts by symbiotic or pathogenic. AI-2 is produced by a range of Gram-positive and Gram-negative bacteria [11, 12] and regulates bioluminescence, biofilm formation, motility, and virulence [13] Most of these functions have been investigated in communities of individual species, several studies suggested the importance of interspecies communication mediated by AI-2 for establishment of mixed biofilms and development of dental plaque [14,15,16]. AI-2 is produced by many gut-associated bacteria [17,18,19], and it was shown to affect the composition of the gut microbiota, favoring Firmicutes while hindering Bacteroides in an antibiotic-treated mouse model [20]

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Results

Conclusion