The sociobiology of biofilms

Abstract

Biofilms are densely packed communities of microbial cells that grow on surfaces and surround themselves with secreted polymers. Many bacterial species form biofilms, and their study has revealed them to be complex and diverse. The structural and physiological complexity of biofilms has led to the idea that they are coordinated and cooperative groups, analogous to multicellular organisms. We evaluate this idea by addressing the findings of microbiologists from the perspective of sociobiology, including theories of collective behavior (self-organization) and social evolution. This yields two main conclusions. First, the appearance of organization in biofilms can emerge without active coordination. That is, biofilm properties such as phenotypic differentiation, species stratification and channel formation do not necessarily require that cells communicate with one another using specialized signaling molecules. Second, while local cooperation among bacteria may often occur, the evolution of cooperation among all cells is unlikely for most biofilms. Strong conflict can arise among multiple species and strains in a biofilm, and spontaneous mutation can generate conflict even within biofilms initiated by genetically identical cells. Biofilms will typically result from a balance between competition and cooperation, and we argue that understanding this balance is central to building a complete and predictive model of biofilm formation.

Beyond the Black Queen Hypothesis

“…First, it allows for resistance against environmental changes or perturbation. Second, in a dependency context, helpers are indispensable, which will partly prevent them from being replaced by competing species (Nadell et al, 2009). It is therefore of particular interest to keep, or even to acquire, the status of helper.…”

Evolutionary and population dynamics: A coupled approach

“…This is motivated by the dynamics observed in microbial biofilms where strong forms of cooperation can be observed [51,55,57,59,60,67]. Single individuals produce metabolically costly products which they release into the environment to support, for example, biofilm formation or nutrient depletion.…”

“…Public good scenarios where a metabolically costly biochemical product is shared among individuals are of particular interest from an evolutionary perspective (see, e.g., [51,55,[58][59][60]). This includes, for example, nutrient uptake, like disaccharides in yeast [61][62][63], collective fruiting body formation [64,65], or the active formation of biofilms [52,57,66,67]. An example regarding iron uptake is considered below in more detail [68][69][70].…”

Extracellular matrix structure governs invasion resistance in bacterial biofilms

“…Bacteria collectively construct spatially complex and functionally diverse communities, termed biofilms, which are now known to be a dominant form of microbial life (Hall-Stoodley et al, 2004;West et al, 2006West et al, , 2007aNadell et al, 2009;Hibbing et al, 2010;Xavier, 2011). Biofilmdwelling cells secrete extracellular substances, including nutrient-sequestering compounds, digestive enzymes and structural matrices composed of proteins, DNA and polysaccharides (Arvidson, 2000;Visca et al, 2007;Stewart and Franklin, 2008;Flemming and Wingender, 2010;Stewart, 2012).…”