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.细菌早期表面定殖并非细胞随机附着于表面并增殖的随机过程；相反，附着事件、细胞运动与细胞间相互作用共同催生了非随机的空间组织结构。我们对表观自组织如何影响种群适合度的研究，尚处于起步阶段。影响种群适合度的关键因素之一，是独居浮游型与聚集态表面附着型生物被膜生活方式之间的权衡关系。尽管浮游细菌通常增殖速率更快，但聚集态的细菌对干燥、抗生素及捕食等胁迫的抗性更强。本研究旨在探究在周期性胁迫条件下，经信息引导的表面附着策略能否以及在何种程度上提升早期表面定殖过程中的种群适合度。我们采用基于个体的建模（individual-based modeling）方法，模拟了在干湿交替循环条件下，具有觅食行为的浮游细菌在表面的定殖过程。这类干湿循环广泛存在于地球上最大的陆地微生物生境——土壤、植物根系及叶表——这些生境不会持续处于水饱和状态，且会每日经受干燥胁迫。我们对比了多种表面附着策略，并分析了表面定殖过程中涌现出的时空动态特征，以及作为适合度衡量指标的种群产出量。我们的研究表明，一种针对高密度位点具有附着偏好的简单优先附着（preferential attachment, PA）策略，在广泛的环境条件下——尤其是在周期性胁迫环境中——相较任意随机附着策略均具备显著的适合度优势。