Migration alters oscillatory dynamics and promotes survival in connected bacterial populations

Gokhale, Shreyas; Conwill, Arolyn; Ranjan, Tanvi; Gore, Jeff

doi:10.1038/s41467-018-07703-y

“…However, it has been difficult to directly connect the empirical observations to theory (25), in part because these natural expansions cannot be replicated, and also because numerous environmental factors cannot be well-controlled. Microcosm experiments have helped address this chasm between theory and experiments by partially trading off realism for much better controlled and replicable biological systems (26)(27)(28)(29)(30).…”

Section: Introductionmentioning

confidence: 99%

Cooperation mitigates diversity loss in a spatially expanding microbial population

Gandhi

¹

,

Korolev

²

,

Gore

³

2019

Preprint

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The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a drastic reduction in diversity during expansions when yeast grows noncooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations. When cells grow independently from each other, the expansion proceeds as a pulled wave driven by the growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the lowdensity tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps. KeywordsRange expansions | Cooperative growth | Serial founder effect | Genetic drift| Allee effect 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Significance statementSpatially expanding populations lose genetic diversity rapidly because of the repeated bottlenecks formed at the front as a result of the serial founder effect.However, the rate of diversity loss depends on the specifics of the expanding population, such as its growth and dispersal dynamics. We have previously demonstrated that changing the amount of within-species cooperation leads to a qualitative transition in the nature of expansion from pulled (driven by migration at the low density tip) to pushed (driven by migration from the high density region at the front, but behind the tip). Here we demonstrate experimentally that pushed waves, which emerge in the presence of sufficiently strong cooperation, result in strongly reduced genetic drift during range expansions, thus preserving genetic diversity in the newly colonized region.

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“…However, it has been difficult to directly connect the empirical observations to theory (22, 26), in part because these natural expansions cannot be replicated, and also because numerous environmental factors cannot be well controlled. Microcosm experiments have helped address this chasm between theory and experiments by partially trading off realism for much better controlled and replicable biological systems (27–31).…”

mentioning

confidence: 99%

Cooperation mitigates diversity loss in a spatially expanding microbial population

Gandhi

¹

,

Korolev

²

,

Gore

³

2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a drastic reduction in diversity during expansions when yeast grows noncooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations: When cells grow independently from each other, the expansion proceeds as a pulled wave driven by growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the low-density tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps.

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“…Optimizing media-or alternatively, resupending cells in PBS or similar media-may improve composition estimates, making the method more widely applicable. But even in the absence of these extensions, the method provides an easily scalable option for competition assays in high-density populations, such as those involving daily "endpoint" measures of composition (43,44,46).…”

Section: Discussionmentioning

confidence: 99%

Fluorescent reporter plasmids for single-cell and bulk-level composition assays inE. faecalis

Hallinen

¹

,

Guardiola-Flores

²

,

Wood

³

2019

Preprint

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ABSTRACTFluorescent reporters are an important tool for monitoring dynamics of bacterial populations at the single cell and community level. While there are a large range of reporter constructs available–particularly for common model organisms like E. coli–fewer options exist for other species, including E. faecalis, a gram-positive opportunistic pathogen. To expand the potential toolkit available for E. faecalis, we modified a previously developed reporter plasmid (pBSU101) to express one of nine different fluorescent reporters and confirmed that all constructs exhibited detectable fluorescence in single E. faecalis cells and mixed biofilm communities. To identify promising constructs for bulk-level experiments, we then measured the fluorescence spectra from E. faecalis populations in microwell plate (liquid) cultures during different growth phases. Cultures showed density- and reporter-specific variations in fluorescent signal, though spectral signatures of all reporters become clear in late-exponential and stationary-phase populations. Based on these results, we identified six pairs of reporters that can be combined with simple spectral unmixing to accurately estimate population composition in 2-strain mixtures at or near stationary phase. This approach offers a simple and scalable method for selection and competition experiments in simple two-species populations. Finally, we modified the construct to express codon-optimized variants of blue (BFP) and red (RFP) reporters and show that they lead to increased fluorescence in exponentially growing cells. As a whole, the results inform the scope of application of different reporters and identify both single reporters and reporter pairs that are promising for fluorescence-based assays at bulk and single-cell levels in E. faecalis.

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Migration alters oscillatory dynamics and promotes survival in connected bacterial populations

Cited by 26 publications

References 65 publications

Cooperation mitigates diversity loss in a spatially expanding microbial population

Cooperation mitigates diversity loss in a spatially expanding microbial population

Cooperation mitigates diversity loss in a spatially expanding microbial population

Fluorescent reporter plasmids for single-cell and bulk-level composition assays inE. faecalis

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