Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations

Abstract

Microbial populations often experience fluctuations in nutrient complexity in their natural environment such as between high molecular weight polysaccharides and simple monosaccharides. However, it is unclear if cells can adopt growth behaviors that allow individuals to optimally respond to differences in nutrient complexity. Here, we directly control nutrient complexity and use quantitative single-cell analysis to study the growth dynamics of individuals within populations of the aquatic bacterium Caulobacter crescentus. We show that cells form clonal microcolonies when growing on the polysaccharide xylan, which is abundant in nature and degraded using extracellular cell-linked enzymes; and disperse to solitary growth modes when the corresponding monosaccharide xylose becomes available or nutrients are exhausted. We find that the cellular density required to achieve maximal growth rates is four-fold higher on xylan than on xylose, indicating that aggregating is advantageous on polysaccharides. When collectives on xylan are transitioned to xylose, cells start dispersing, indicating that colony formation is no longer beneficial and solitary behaviors might serve to reduce intercellular competition. Our study demonstrates that cells can dynamically tune their behaviors when nutrient complexity fluctuates, elucidates the quantitative advantages of distinct growth behaviors for individual cells and indicates why collective growth modes are prevalent in microbial populations.

Polysaccharide-Bacteria Interactions From the Lens of Evolutionary Ecology

“…For example, mucin derived oligosaccharide can inhibit virulence in P. aeruginosa (Wheeler et al, 2019), whereas free fucose cleaved from mucin increase virulence of E. coli (Pacheco et al, 2012). Also, motility can be regulated by cyanobacterial mucin and derived oligosaccharides (Reddi et al, 2018) or xylose in Caulobacter crescentus (D'Souza et al, 2021). However, there is still much to learn about the potential for oligosaccharides to act as control "knobs" of bacterial behavior.…”

Cryptic surface-associated multicellularity emerges through cell adhesion and its regulation

“…Competition experiments revealed that spatial interactions can strongly affect the outcome of competition, oftentimes leading to the coexistence of multiple genotypes [ 43 , 120 , 125 ]. However, due to technical challenges and the transient nature of many primitive cell collectives [ 126 ], there is often a limited quantitative understanding of how genotypes exactly give rise to individual cell collectives and how these collectives subsequently grow and propagate in competition with other collectives. Since the spatiotemporal organization of collectives determines a genotype’s competitive success (i.e., rates of collective growth and reproduction)—making collectives the relevant unit of biological organization [ 49 , 50 ]—we need to understand how collective organization comes about to uncover how primitive forms of surface-associated multicellularity first arise and subsequent evolve.…”

“…Fortunately, over the last decade, methods of empirical lineage tracking have strongly improved through advances in single-cell microscopy [126][127][128], image analysis [129], singlecell sequencing [51,130,131], and genome editing [132,133], thereby opening up the possibility of studying primitive cell collectives across a wide range of organisms [126]. For example, the stochastic and combinatorial expression of fluorescent proteins makes it possible to trace up to approximately 100 lineages without interrupting the spatial configuration of cells [134].…”

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

“…Diversity and quantity of nutrients might be two understudied factors that drive ecology and genome size evolution. A recent example shows that polysaccharide xylan triggers microcolonies, whereas monosaccharide xylose promotes solitary growth in Caulobacter (62). This is a striking example of how nutrient complexity can foster diverse niches for well-studied cells such as Caulobacter with genome size 4 Mb.…”