An evolutionarily stable strategy to colonize spatially extended habitats

Liu, Weirong; Cremer, Jonas; Li, Dengjin; Hwa, Terence; Liu, Chenli

doi:10.1038/s41586-019-1734-x

Cited by 52 publications

(75 citation statements)

References 50 publications

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“…This bi-phasic growth pattern, which was most pronounced on pectin, resembles previously described models in motile E. coli, which depicted an initial expansion phase, where "pioneer" bacteria with high velocity advance in front of the colony, followed by a second phase, where "settler" bacteria grow and replicate locally (16,69).…”

Section: Discussionsupporting

confidence: 83%

Pectin induced colony expansion of soil-derived Flavobacterium strains

Kraut-Cohen¹,

Shapiro

Dror

et al. 2020

Preprint

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Flavobacterium is a genus of gram-negative bacteria, belonging to the Bacteriodetes phylum, characterized by a unique gliding motility. They are ubiquitous and often abundant in root microbiomes of various plants, but the factors contributing to this high abundance are currently unknown. In this study, we evaluate the effect of various plant-associated poly- and mono-saccharides on growth and colony expansion of two Flavobacterium strains (F. Johnsoniae, Flavobacterium sp. F52). Both strains were able to grow on pectin and other polysaccharides such as cellulose as a single carbon source. However, only pectin, a polysaccharide that is profuse in plant cell walls, enhanced colony expansion on solid surfaces even under high nutrient availability, suggesting a link between carbohydrate metabolism and gliding. Expansion on pectin was dose- and substrate-dependent, as it did not occur when bacteria were grown on the pectin monomers galacturonic acid and rhamnose. Using time-lapse microscopy, we demonstrated a bi-phasic expansion of F. johnsoniae on pectin: an initial phase of rapid expansion, followed by biomass production within the colonized area. Proteomics and gene expression analyses revealed significant induction of several carbohydrate metabolism related proteins when F. johnsoniae was grown on pectin, including selected operons of SusC/D, TonB-dependent glycan transport genes. Our results suggest a yet unknown linkage between specific glycan associated operons and flavobacterial motility. This may be associated with their capacity to rapidly glide along the root and metabolize plant cell wall carbohydrates, two characteristics that are crucial to rhizosphere competence.ImportanceThe genus Flavobacterium is highly abundant and enriched (relative to surrounding bulk soil) in plant root microbiomes, where they may play a role in plant health and ecosystem functioning. However, little is known about genetic and physiological characteristics that enable flavobacteria to colonize and proliferate in this highly competitive environment. In this study, we found that plant cell wall-polysaccharides and specifically pectin stimulate flavobacteria colony development in a bi-phasic manner, initially characterized by rapid expansion followed by increased biomass production. This appears to be linked to pectin-facilitated induction of specific TonB-associated proteins evidentially involved in the detection and uptake of plant sugars. These findings suggest that the capacity to sense, expand on and metabolize pectin and other plant cell wall polysaccharides play a fundamental role in promoting rhizosphere competence in flavobacteria. This work sheds light on specific mechanisms that facilitate plant-microbe interactions, which are fundamental for promoting plant health and for understanding the microbial ecology of root ecosystems.

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Section: Discussionsupporting

confidence: 83%

Pectin induced colony expansion of soil-derived Flavobacterium strains

Kraut-Cohen¹,

Shapiro

Dror

et al. 2020

Preprint

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“…The measurement allows for the spatiotemporal resolution of swimming behavior within an expanding population. To optimize the tracking of single cells, the number of fluorescent detecetable cells was adjusted by mixing fluorescent cells with non-flucorescent cells (carrying a non-fluorescence protein 59 to minimize physiological differences of strains). Detailed methods on image acquisition, cell tracking and the statistical analysis to derive diffusion coefficients and drift are given in Supplementary Text 1.5.…”

Section: Cell Trajectory Analysis In Soft Agarmentioning

confidence: 99%

Chemotaxis as a navigation strategy to boost range expansion

Cremer

Honda

Tang

et al. 2019

Nature

Self Cite

126

224

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Bacterial chemotaxis, the directed movement of cells along "chemoattractant" gradients, is among the best-characterized subjects of molecular biology 1-10. Much less is known about its physiological roles 11. Commonly, it is seen as starvation response when nutrients run out, or as escape response from harmful situations 12-16. Here, we establish an alternative role of chemotaxis by systematically examining the spatiotemporal dynamics of Escherichia coli in soft agar 12,17,18 : Chemotaxis in nutrient-replete conditions promotes the expansion of bacterial populations into unoccupied territories well before nutrients run out in the current environment. We show how low levels of chemoattractants act as aroma-like cues in this process, establishing the direction and enhancing the speed of population movement along the self-generated attractant gradients. This navigated range expansion process spreads faster and yields larger population gains than unguided expansion following the canonical Fisher-Kolmogorov dynamics 19,20 and is therefore a general strategy to promote population growth in spatially extended, nutrient-replete environments.

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“…2 and 3). Previous studies have shown that expansion speed could be also influenced by interactions among differentiated pioneering cells at the front of the expanding population [26]. However, in this study the standing variation in the ancestral population is expected to be low, and interactions between different cell types is therefore potentially limited.…”

Section: Discussionmentioning

confidence: 87%

Dissection of the mutation accumulation process during bacterial range expansions

et al. 2020

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Background: Recent experimental work has shown that the evolutionary dynamics of bacteria expanding across space can differ dramatically from what we expect under well-mixed conditions. During spatial expansion, deleterious mutations can accumulate due to inefficient selection on the expansion front, potentially interfering with and modifying adaptive evolutionary processes. Results: We used whole genome sequencing to follow the genomic evolution of 10 mutator Escherichia coli lines during 39 days (~1650 generations) of a spatial expansion, which allowed us to gain a temporal perspective on the interaction of adaptive and non-adaptive evolutionary processes during range expansions. We used elastic net regression to infer the positive or negative effects of mutations on colony growth. The colony size, measured after three day of growth, decreased at the end of the experiment in all 10 lines, and mutations accumulated at a nearly constant rate over the whole experiment. We find evidence that beneficial mutations accumulate primarily at an early stage of the experiment, leading to a non-linear change of colony size over time. Indeed, the rate of colony size expansion remains almost constant at the beginning of the experiment and then decreases after~12 days of evolution. We also find that beneficial mutations are enriched in genes encoding transport proteins, and genes coding for the membrane structure, whereas deleterious mutations show no enrichment for any biological process. Conclusions: Our experiment shows that beneficial mutations target specific biological functions mostly involved in inter or extra membrane processes, whereas deleterious mutations are randomly distributed over the whole genome. It thus appears that the interaction between genetic drift and the availability or depletion of beneficial mutations determines the change in fitness of bacterial populations during range expansion.

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An evolutionarily stable strategy to colonize spatially extended habitats

Cited by 52 publications

References 50 publications

Pectin induced colony expansion of soil-derived Flavobacterium strains

Pectin induced colony expansion of soil-derived Flavobacterium strains

Chemotaxis as a navigation strategy to boost range expansion

Dissection of the mutation accumulation process during bacterial range expansions

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