Collective colony growth is optimized by branching pattern formation in Pseudomonas aeruginosa

Abstract

Branching pattern formation is common in many microbes. Extensive studies have focused on addressing how such patterns emerge from local cell-cell and cell-environment interactions. However, little is known about whether and to what extent these patterns play a physiological role. Here, we consider the colonization of bacteria as an optimization problem to find the colony patterns that maximize colony growth efficiency under different environmental conditions. We demonstrate that Pseudomonas aeruginosa colonies develop branching patterns with characteristics comparable to the prediction of modeling; for example, colonies form thin branches in a nutrient-poor environment. Hence, the formation of branching patterns represents an optimal strategy for the growth of Pseudomonas aeruginosa colonies. The quantitative relationship between colony patterns and growth conditions enables us to develop a coarse-grained model to predict diverse colony patterns under more complex conditions, which we validated experimentally. Our results offer new insights into branching pattern formation as a problem-solving social behavior in microbes and enable fast and accurate predictions of complex spatial patterns in branching colonies.

Morphological instability and roughening of growing 3D bacterial colonies

“…Some of these patterns become 3D as the colony can grow and deform into the third dimension. These morphologies are now understood to arise from friction between the growing colony and the surface and differential access to nutrients, which may also be available from the third dimension ( 13 – 18 , 20 , 22 – 26 ). The emergent patterns have been rationalized by incorporating these key ingredients into reaction–diffusion equations ( 14 – 16 , 18 , 22 , 27 – 36 ), active continuum theories ( 19 – 21 , 28 , 31 , 37 – 53 ), and agent-based models ( 28 , 31 , 38 , 40 , 45 , 46 , 54 – 57 ).…”

Roughening instability of growing 3D bacterial colonies

“…Some of these patterns become 3D as the colony can grow and deform into the third dimension. These morphologies are now understood to arise from friction between the growing colony and the surface, and differential access to nutrients, which may also be available from the third dimension [14–20, 22, 24–28]. The emergent patterns have been rationalized by incorporating these key ingredients into reaction-diffusion equations [2, 15–18, 20, 24, 29–36], active continuum theories [21–23, 30, 32, 37–50], and agent-based models [30, 32, 38, 40, 45, 46, 51–54].…”

Self-organized canals enable long range directed material transport in bacterial communities

“…Flow profile measurement and mathematical modeling that involves multiple transport processes and quorum-sensing (QS) regulation (Mukherjee & Bassler, 2019) together reveal the spatial-temporal dynamics of fluid flows in bacterial canals. Overall, our findings demonstrate that mechanochemical coupling between interfacial force and biosurfactant kinetics can coordinate large-scale material transport in primitive life forms, advancing the understanding on multicellular microbial behavior and suggesting a new principle to design macroscopic patterns and functions of synthetic microbial communities (Brenner, You, & Arnold, 2008; Chen, Kim, Hirning, Josić, & Bennett, 2015; Kong, Meldgin, Collins, & Lu, 2018; Luo, Wang, Lu, Ouyang, & You, 2021; Miano, Liao, & Hasty, 2020).…”

“…In our current study, cell mass transported by canals may contribute to colony expansion but this is not always the case (e.g., see Movie S4); more importantly, the speed of directed transport via canals occurring inside the colony is two orders of magnitude greater than that of typical colony expansion (∼200 µm/s versus ∼2 mm/hr). Nonetheless, our work provides an new ingredient (i.e., long-range material transport driven by interfacial mechanics) that will complement existing models such as fingering instability (Trinschek et al, 2018) and colony-growth optimization (Luo et al, 2021) to explain and control pattern formation in expanding P. aeruginosa colonies.…”