Spatially Correlated Gene Expression in Bacterial Groups: The Role of Lineage History, Spatial Gradients, and Cell-Cell Interactions

Vliet, Simon van; Co, Alma Dal; Winkler, Annina R.; Spriewald, Stefanie; Stecher, Bärbel; Ackermann, Martin

doi:10.1016/j.cels.2018.03.009

Cited by 64 publications

(74 citation statements)

References 68 publications

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“…First, plasmid copy number variation could lead to overestimate the variation in gene expression between cells. However, previous work has shown that for most promoters copy number variation of the reporter plasmids we used is negligible compared to variation in transcriptional activity [33,34]. Second, because (fluorescent) proteins have long lifetimes, fluorescent intensities in cells do not only depend on current, but also on past, transcriptional activity.…”

Section: Resultsmentioning

confidence: 98%

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Ackermann

Vliet

2019

Preprint

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Microbes live in ever-changing environments where they need to adapt their metabolism to different nutrient conditions. Many studies have characterized the response of genetically identical cells to nutrient switches in homogenous cultures, however in nature microbes often live in spatially structured groups such as biofilms where cells can create metabolic gradients by consuming and releasing nutrients. Consequently, cells experience different local microenvironments and vary in their phenotype. How does this phenotypic variation affect the ability of cells to cope with nutrient switches? Here we address this question by growing dense populations of Escherichia coli in microfluidic chambers and studying a switch from glucose to acetate at the single cell level. Before the switch, cells vary in their metabolic activity: some grow on glucose while others cross-feed on acetate. After the switch, only few cells can resume growth after a period of lag. The probability to resume growth depends on a cells' phenotype prior to the switch: it is highest for cells crossfeeding on acetate, while it depends in a non-monotonic way on growth rate for cells growing on glucose. Our results suggest that the strong phenotypic variation in spatially structured populations might enhance their ability to cope with fluctuating environments.

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Section: Resultsmentioning

confidence: 98%

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Ackermann

Vliet

2019

Preprint

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“…Verifying the proportion of SAR11 cells actively dividing in a culture may be challenging. Time-lapse microscopy (135) offers an elegant solution if SAR11 can be maintained for the requisite time periods for accurate measurements in a microfluidic device.…”

Section: Discussionmentioning

confidence: 99%

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

Henson

Lanclos

Pitre

et al. 2020

Preprint

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48Cultivated representatives of bacterioplankton from diverse lineages and locations are 49 essential for experimentally determining the physiology and metabolism that influences their 50 distributions and ecological functions. Despite widespread efforts to bring more microorganisms 51 into culture, the large majority of taxa either remain uncultivated or lack isolates from diverse 52 geographic locales. Furthermore, we have little understanding of the factors that influence 53 relative cultivation success for any particular taxon. We paired large scale dilution-to-extinction 54 (DTE) cultivation with microbial community analysis and DTE modeling to expand the 55 phylogenetic and geographic diversity of cultivated bacterioplankton and to evaluate the success 56 of DTE cultivation for isolating abundant taxa. Here we report the results from 17 DTE 57 experiments totaling 7,820 individual incubations over three years that resulted in 328 repeatably 58 transferable cultures. Comparison of isolates to microbial community taxonomic profiles of 59 source waters indicated that we successfully isolated 5% of the observed bacterioplankton taxa 60 across all 17 sites. 43% and 26% of our isolates matched operational taxonomic units (OTUs) 61 and amplicon single nucleotide variants (ASVs), respectively, within the top 50 most abundant 62 taxa observed during the study. Isolates included those from previously uncultivated clades such 63 as SAR11 LD12 and Actinobacteria acIV, as well as geographically novel members from other 64 ecologically important groups like SAR11 subclade III, HIMB59 Alphaproteobacteria, SAR116, 65OM43, and HIMB11-type Roseobacter spp.. The effort resulted in the first isolates in eight 66 genera and seven species. We also developed a new model of DTE cultivation to evaluate 67 viability of taxa based on the relationship between relative abundance and cultivation success. 68The model i) revealed minimum levels of wells required for successful isolation of taxa 69 amenable to growth on our media, and ii) identified several important and abundant taxa such as 70 SAR11 with low viability that likely impacts cultivation success. By incorporating predicted, 71 measured, or assumed viability in an iterative manner, we can now provide a statistically 72 constrained number of attempts necessary for successful cultivation of a given taxon on a defined 73 medium based on relative abundance. 74 75 76 Importance 77Even before the coining of the term "great plate count anomaly" in the 1980s, scientists 78 had noted the discrepancy between the number of microorganisms observed under the 79 microscope and the number of colonies that grew on traditional agar media. New cultivation 80 approaches have reduced this disparity, resulting in the isolation of some of the "most wanted" 81 bacterial lineages. Nevertheless, the vast majority of microorganisms remain uncultured, 82 hampering progress towards answering fundamental biological questions about many important 83 microorganisms. Furthermore, few studies have evaluate...

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“…Growth rates were log transformed. GFP_vecfw 5' CAC TGG AGT TGT CCC AAT TCT TGT TG pSV66-rpsM-gfp-rpsM-rfp [3] RFP_vec-rv 5' ATG AGC GAG CTG ATC AAG G pSV66-rpsM-gfp-rpsM-rfp [3] GFP_vec-rv 5' GTT TCT TAG ACG TCG GAA TTG CCA G pSV66-rpsM-gfp-rpsM-rfp [3] RFP_vecfw 5' CTG TTC TGG TGT TGC TAG TTT G pSV66-rpsM-gfp-rpsM-rfp [3] Supplemental references…”

Section: Supplemental Moviementioning

confidence: 99%

Emergent microscale gradients give rise to metabolic cross-feeding and antibiotic tolerance in clonal bacterial populations

Vliet

Ackermann

2019

Phil. Trans. R. Soc. B

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Supplemental Figure 1. Nutrient gradients and gene expression are reproducible across replicates. The figure shows the profiles of single cell growth rate (left), normalized ptsG expression (middle), and normalized acs expression (right) for wildtype (WT, top) and acs mutant populations (bottom), each line shows average values within a single replicate (six to ten chambers). Note that overall profiles are very similar between replicates, though some are shifted slightly towards higher or lower depth (e.g. dark gray line acs mutant). This is likely due to slight variation in the density of cells, chamber height, or flow pressure that can change how deep glucose can penetrate into the chamber before being depleted.

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Spatially Correlated Gene Expression in Bacterial Groups: The Role of Lineage History, Spatial Gradients, and Cell-Cell Interactions

Cited by 64 publications

References 68 publications

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

Emergent microscale gradients give rise to metabolic cross-feeding and antibiotic tolerance in clonal bacterial populations

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