Multi-species biofilms: how to avoid unfriendly neighbors Olaya Rendueles, Jean-Marc Ghigo To cite this version: Olaya Rendueles, Jean-Marc Ghigo. Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiology Reviews, Wiley-Blackwell, 2012, 36 (5), pp.972-989. 10.1111/j.1574-6976.2012.00328.x. hal-02613136 HAL Id: hal-02613136 https://hal.archives-ouvertes.fr/hal-02613136 Submitted on 8 Jul 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW ARTICLE Multi-species biofilms: how to avoid unfriendly neighbors Olaya Rendueles & Jean-Marc Ghigo Institut Pasteur, Unite´ de Ge´ ne´ tique des Biofilms, Paris, France Correspondence: Jean-Marc Ghigo, Institut Abstract Pasteur, Unite´ de Ge´ ne´ tique des Biofilms, 25-28 rue du Dr Roux, 75724 Paris Cedex Multi-species biofilm communities are environments in which complex but ill 15, France. Tel.: +33 01 40 61 34 18; understood exchanges between bacteria occur. Although monospecies cultures fax: +33 01 45 68 88 36; are still widely used in the laboratory, new approaches have been undertaken e-mail: [email protected] to study interspecies interactions within mixed communities. This review describes our current understanding of competitive relationships involving Received 12 October 2011; revised 17 nonbiocidal biosurfactants, enzymes, and metabolites produced by bacteria and December 2011; accepted 22 December 2011. Final version published online 8 March other microorganisms. These molecules target all steps of biofilm formation, 2012. ranging from inhibition of initial adhesion to matrix degradation, jamming of cell–cell communications, and induction of biofilm dispersion. This review pre- DOI: 10.1111/j.1574-6976.2012.00328.x sents available data on nonbiocidal molecules and provides a new perspective on competitive interactions within biofilms that could lead to antibiofilm strat- Editor: Dieter Haas egies of potential biomedical interest. Keywords biofilm formation; adhesion; bacterial interferences; mixed communities; biosurfactants; biofilm dispersion. However, biofilm formation is a complex process Introduction involving multiple adhesion and dispersion events which, In most environments, bacteria form multispecies com- from initial surface contact to tri-dimensional matura- munities and develop heterogeneous structures known as tion, can be shaped by microbial interactions that do not biofilms (Costerton et al., 1987; Hall-Stoodley et al., necessarily rely on growth-inhibiting molecules or pro- 2004). In contrast to liquid suspensions, the high cell den- cesses (Fig. 1). Recently, the studies on mixed biofilm sity and reduced diffusion prevailing within biofilms pro- communities have shed light on a surprising diversity of vide opportunities for intense exchanges ranging from nonbiocidal compounds targeting different stages of bio- cooperation (for a detailed review of cooperative interac- film formation (Table 1). Although most of these com- tions see the accompanying paper by Elias and Banin pounds were first identified in monospecies cultures or appearing in this issue) to harsh competition (James et al., studied in ecologically irrelevant experimental mixed spe- 1995; Moons et al., 2009). Such interactions can lead to cies settings, they could be involved in biofilm population physiological and regulatory alterations within biofilm dynamics in vivo. This review describes how nonbiocidal bacteria, and this may eventually contribute to the selec- molecules affect microbial interactions in biofilm environ- tion of better adapted mutants. These interactions can ments and discusses their potential biological role and influence the emergence and disappearance of species and perspectives as alternative antibiofilm molecules of indus- therefore play an important role in the shaping of multi- trial and biomedical interest. species biofilm communities (Hibbing et al., 2010; Dubey & Ben-Yehuda, 2011). Thus far, the studies of how bacte- A cold welcome: Inhibition of initial MICROBIOLOGY REVIEWS MICROBIOLOGY ria relate to each other within these communities have adhesion often focused on antagonisms impairing fitness of bacte- rial competitors via, for instance, the production of toxins, The first interactions between bacteria and surfaces are scavenger molecules, and antimicrobials. crucial for biofilm formation and, depending on the ª 2012 Federation of European Microbiological Societies FEMS Microbiol Rev 36 (2012) 972–989 Published by Blackwell Publishing Ltd. All rights reserved Nonbiocidal antibiofilm molecules 973 Fig. 1. Antibiofilm molecules act at several stages of the biofilm formation process. Biofilm formation is often described as a multistep process in which bacteria adhere to an abiotic or biotic surface, through surface charges and production of pili, fimbriae, and exopolysaccharides. After initial attachment, three-dimensional development starts with the building of microcolonies, in which different species already interact. The next step, biofilm maturation, is dependent on matrix production, which ensures cohesion and the three-dimensional structure of mature biofilms (Flemming & Wingender, 2010a). Scanning electron microscopy images representative of each steps are shown. The final step in biofilm formation is cellular detachment or dispersion, by which bacteria regain the planktonic lifestyle to colonize other surfaces. Microbial interferences can inhibit biofilm formation or enhance biofilm dispersion through different mechanisms and strategies at different stages of their development. nature of the surface, can be driven by different mecha- This strategy is illustrated in competition experiments nisms. Adhesion to abiotic surfaces, for instance, is often between Pseudomonas aeruginosa and Agrobacterium tum- mediated by nonspecific events that primarily depend on efaciens (An et al., 2006). In a mixed species co-cultiva- cell-surface charge and hydrophobicity, the presence of tion experimental model, P. aeruginosa rapidly spread extracellular polymers and organic conditioning film through the surface via swarming and twitching motility, (Dunne, 2002). On the other hand, binding to biotic sur- preventing A. tumefaciens adhesion. In contrast, a P. aeru- faces such as host tissues and mucosa epithelial cells can ginosa flgK motility-deficient mutant unable to spread be mediated by specific receptors and influenced by host quickly over a surface was no longer able to exclude A. tum- responses to bacterial colonization (Finlay & Falkow, efaciens, therefore allowing A. tumefaciens to form a mixed 1989; Kline et al., 2009). While environmental factors surface biofilm with P. aeruginosa (An et al., 2006). influence the initial steps of adhesion, bacterial activity Although this simple and intuitive strategy is often per se has also been shown to alter the outcome of surface mentioned as a possible competition mechanism, the actual interactions through either production of antiadhesion contribution of surface blanketing in interspecies interac- molecules that modify surface physico-chemical proper- tions is currently not known. ties, or composition of a physical bacterial barrier (sur- face ‘blanketing’) preventing surface contact with other Slippery surface: biosurfactant production competing bacteria. Bacteria have long been known to secrete biosurfactants altering surface properties such as wettability and charge Bacterial surface blanketing (Neu, 1996; Banat et al., 2010). The physiological roles of One of the simplest strategies for avoiding initial coloni- these surfactants, widespread among bacteria, are often zation of competing strains is the rapid occupancy of all unclear, but they generally weaken bacteria-surface and available adhesion sites, referred to as ‘surface blanketing’. bacteria–bacteria interactions, therefore reducing the ability FEMS Microbiol Rev 36 (2012) 972–989 ª 2012 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved 974 O. Rendueles & J.-M. Ghigo Table 1. Biofilm-inhibiting molecules produced by other bacteria. Different colors indicate successive stages of the biofilm life cycle ª 2012 Federation of European Microbiological Societies FEMS Microbiol Rev 36 (2012) 972–989 Published by Blackwell Publishing Ltd. All rights reserved Nonbiocidal antibiofilm molecules 975 Table 1. Continued ? of bacteria and possibly other microorganisms to form and strains (Kuiper et al., 2004). Uropathogenic extraintestinal colonize biofilms (Rodrigues et al., 2006b, c; Valle et al., E. coli, on the other hand, were shown to prevent biofilm 2006; Walencka et al., 2008b; Rivardo et al., 2009; Jiang formation of a wide range of Gram-positive and Gram-neg- et al., 2011; Rendueles et al., 2011). For instance, the ative bacteria because of the release of group 2 capsule, a well-known surfactin, which is required for Bacillus subtilis high molecular weight polysaccharide encoded by the kps swarming, also inhibits biofilm formation of different locus (Valle et al., 2006; Whitfield, 2006). Group 2 capsule strains, including Escherichia coli, Proteus