A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms

Abstract

Bacteria commonly grow in densely populated surface-bound communities, termed biofilms, where they gain benefits including superior access to nutrients and resistance to environmental insults. The secretion of extracellular polymeric substances (EPS), which bind bacterial collectives together, is ubiquitously associated with biofilm formation. It is generally assumed that EPS secretion is a cooperative phenotype that benefits all neighboring cells, but in fact little is known about the competitive and evolutionary dynamics of EPS production. By studying Vibrio cholerae biofilms in microfluidic devices, we show that EPS-producing cells selectively benefit their clonemates and gain a dramatic advantage in competition against an isogenic EPS-deficient strain. However, this advantage carries an ecological cost beyond the energetic requirement for EPS production: EPS-producing cells are impaired for dispersal to new locations. Our study establishes that a fundamental tradeoff between local competition and dispersal exists among bacteria. Furthermore, this tradeoff can be governed by a single phenotype.

Cutting through the complexity of cell collectives

“…As the biofilm grows, many cell lineages are cut off from access to nutrients due to chance alone, leading to an overall reduction in the number of cell lineages in the biofilm. The lineages that remain become spatially segregated as the cells within them grow and divide [44][45][46]. This effect has been demonstrated experimentally for bacteria [44,47,48], unicellular yeast [47] and social slime moulds [49], and it is conceptually linked to genetic drift of neutral variants and selective sweeps of strains that differ in their reproductive rates [47,48,50,51].…”

“…We now test the predictive role of B L with simulations of biofilms in two-dimensional space. The computational rspb.royalsocietypublishing.org Proc R Soc B 280: 20122770 framework used to run these simulations has previously been described in detail and tested experimentally [34,46,88]. Our model relaxes some of the assumptions of the analytical derivations above by adding realistic detail to the cells and their interactions with each other.…”

Extracellular matrix structure governs invasion resistance in bacterial biofilms

“…A DhapR DflaA double deletion mutant (Nadell and Bassler, 2011), which secretes copious extracellular matrix, was used to produce resident biofilms. We refer to this strain as 'Rugose' (Yildiz et al, 2004), as it forms wrinkled colonies on agar.…”

The evolution of the competition–dispersal trade-off affects α- and β-diversity in a heterogeneous metacommunity

“…In this context, resource partitioning plays an important role, but numerous theoretical [4][5][6] and experimental [7,8] studies have emphasized that trade-offs between local competitive ability and dispersal of species in patchy environments (so-called competition-colonization or competition-dispersal trade-offs) also favour coexistence. Both empirical studies and field surveys suggest that these trade-offs are a distinctive characteristic of communities from many natural systems [9,10], and are sometimes associated with wide variation in dispersal among species belonging to the same community (e.g. [11] for the tree community of Barro Colorado Island).…”