Bacterial surface colonization, preferential attachment and fitness under periodic stress

Early bacterial surface colonization is not a random process wherein cells arbitrarily attach to surfaces and grow; but rather, attachment events, movement and cellular interactions induce non-random spatial organization. We have only begun to understand how the apparent self-organization affects the fitness of the population. A key factor contributing to fitness is the tradeoff between solitary-planktonic and aggregated surface-attached biofilm lifestyles. Though planktonic cells typically grow faster, bacteria in aggregates are more resistant to stress such as desiccation, antibiotics and predation. Here we ask if and to what extent informed surface-attachments improve fitness during early surface colonization under periodic stress conditions. We use an individual-based modeling approach to simulate foraging planktonic cells colonizing a surface under alternating wet-dry cycles. Such cycles are common in the largest terrestrial microbial habitats–soil, roots, and leaf surfaces–that are not constantly saturated with water and experience daily periods of desiccation stress. We compared different surface-attachment strategies, and analyzed the emerging spatio-temporal dynamics of surface colonization and population yield as a measure of fitness. We demonstrate that a simple strategy of preferential attachment (PA), biased to dense sites, carries a large fitness advantage over any random attachment across a broad range of environmental conditions–particularly under periodic stress.Author summary: A vast portion of bacterial life on Earth takes place on surfaces. In many of these surfaces cells collectively organize into biofilms that are known to provide them protection from various environmental stresses. Early bacterial colonization of surfaces, prior to the development of mature biofilm, is a critical stage during which cells attempt to establish a sustainable population. It is not a random process wherein cells arbitrarily attach to surfaces and grow to form micro-colonies. Rather, surface-attachments, movement and cellular interactions take place to yield non-random organization. Using computer simulations, based on individual-based modeling, we demonstrate that simple attachment strategies, where planktonic cells preferentially attach to existing surface-attached aggregates, may confer fitness advantage over random attachment. The advantage of preferential attachment is particularly substantial under periodic stress–a common characteristic of many natural microbial habitats. This is due to a more efficient recruitment of planktonic cells that accelerates the formation of stress-protected aggregates.