Abstract
Interspecific interactions within biofilms determine relative species abundance, growth dynamics, community resilience, and success or failure of invasion by an extraneous organism. However, deciphering interspecific interactions and assessing their contribution to biofilm properties and function remain a challenge. Here, we describe the constitution of a model biofilm composed of four bacterial species belonging to four different genera (Rhodocyclus sp., Pseudomonas fluorescens, Kocuria varians, and Bacillus cereus), derived from a biofilm isolated from an industrial milk pasteurization unit. We demonstrate that the growth dynamics and equilibrium composition of this biofilm are highly reproducible. Based on its equilibrium composition, we show that the establishment of this four‐species biofilm is highly robust against initial, transient perturbations but less so towards continuous perturbations. By comparing biofilms formed from different numbers and combinations of the constituent species and by fitting a growth model to the experimental data, we reveal a network of dynamic, positive, and negative interactions that determine the final composition of the biofilm. Furthermore, we reveal that the molecular determinant of one negative interaction is the thiocillin I synthesized by the B. cereus strain, and demonstrate its importance for species distribution and its impact on robustness by mutational analysis of the biofilm ecosystem.
Highlights
In contrast to typical laboratory conditions of growth in liquid culture, bacteria in natural environments and those contaminating hospitals, or industrial and food-processing procedures are more often found in multicellular surface-associated communities known as biofilms (Costerton et al, 1987; Hall-Stoodley et al, 2004; Flemming et al, 2016)
Construction of a multispecies, model biofilm based on a natural ecosystem
Multispecies biofilm we exploited an industrial biofilm consortium, isolated from an industrial food preparation device (Mettler and Carpentier, 1997), comprising 13 strains corresponding to 7 species belonging to 5 genera (Table 1)
Summary
In contrast to typical laboratory conditions of growth in liquid culture, bacteria in natural environments and those contaminating hospitals, or industrial and food-processing procedures are more often found in multicellular surface-associated communities known as biofilms (Costerton et al, 1987; Hall-Stoodley et al, 2004; Flemming et al, 2016). Such biofilms are generally complex communities harboring numerous bacterial species in close spatial proximity (Elias and Banin, 2012). Studies on multispecies biofilms have reported enhanced stress resistance, productivity, or biomass production (Burmølle et al, 2006; Lee et al, 2014; Ren et al, 2015; Liu et al, 2019), and, importantly, "community-intrinsic properties" (Madsen et al, 2018) emerging from the social interactions between members of the biofilm and which may be important for its interaction with its environment
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