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Bacteria can grow in a free-swimming state, as planktonic cells, or in surface-attached communities, termed biofilms. The planktonic and biofilm growth modes differ dramatically with respect to spatial constraints, nutrient access, population density and cell-cell interactions. Fitness trade-offs underlie how successfully bacteria compete in each of these environments. Accordingly, some bacteria have evolved to be specialists in biofilm formation, while others specialize in planktonic growth. There are species, however, that possess flexible strategies: they can transition between the molecular programs required for biofilm formation and for planktonic growth. Such flexible strategies often sacrifice competitive ability against specialists in a given habitat. There is little exploration of the ecological conditions favoring the evolution of the flexible biofilm production strategy for bacteria in competition with specialist biofilm producers or specialist non-producers. Here, we study the human pathogen Vibrio cholerae, a flexible biofilm-former, as well as constitutive biofilm-producing and non-producing mutants. We assess the fitness of these strains under biofilm conditions, planktonic conditions and conditions that demand the ability to transition between the two growth modes. We show that, relative to the specialists, the wild type is superior at dispersal from biofilms to the planktonic phase; however, this capability comes at the expense of reduced competitive fitness against constitutive biofilm producers on surfaces. Wild-type V. cholerae can outcompete the constitutive biofilm producers and non-producers if habitat turnover is sufficiently frequent. Thus, selection for phenotypic flexibility in biofilm production depends on the frequency of environmental fluctuations encountered by bacteria.

Environmental fluctuation governs selection for plasticity in biofilm production