Phenotypic heterogeneity of microbial populations under nutrient limitation

2020 ◽  
Vol 62 ◽  
pp. 160-167 ◽  
Author(s):  
Ana Gasperotti ◽  
Sophie Brameyer ◽  
Florian Fabiani ◽  
Kirsten Jung
Keyword(s):  
Nutrient Limitation ◽  
Phenotypic Heterogeneity ◽  
Microbial Populations

scholarly journals Crosstalk between guanosine nucleotides regulates cellular heterogeneity in protein synthesis during nutrient limitation

2021 ◽  
Author(s):  
Simon Diez ◽  
Molly Hydorn ◽  
Abigail Whalen ◽  
Jonathan Dworkin
Keyword(s):  
Protein Synthesis ◽  
Bacillus Subtilis ◽  
Nutrient Limitation ◽  
Dynamic Environments ◽  
Phenotypic Heterogeneity ◽  
Cellular Heterogeneity ◽  
Microbial Populations ◽  
Low Protein ◽  
Synthesis Activity

Phenotypic heterogeneity of microbial populations can facilitate survival in dynamic environments by generating sub-populations of cells that may have differential fitness in a future environment. Bacillus subtilis cultures experiencing nutrient limitation contain distinct sub-populations of cells exhibiting either comparatively high or low protein synthesis activity. This heterogeneity requires the production of phosphorylated guanosine nucleotides (pp)ppGpp by three synthases: SasA, SasB, and RelA. Here we show that these enzymes differentially affect this bimodality: RelA and SasB are necessary to generate the sub-population of cells exhibiting low protein synthesis whereas SasA is necessary to generate cells exhibiting comparatively higher protein synthesis. The RelA product (pppGpp) allosterically activates SasB and we find, in contrast, that the SasA product (pGpp) competitively inhibits this activation. Finally, we provide in vivo evidence that this antagonistic interaction mediates the observed heterogeneity in protein synthesis. This work therefore identifies the mechanism underlying phenotypic heterogeneity in the central physiological process of protein synthesis.

scholarly journals Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments

2016 ◽  
Vol 1 (6) ◽  
Author(s):  
Frank Schreiber ◽  
Sten Littmann ◽  
Gaute Lavik ◽  
Stéphane Escrig ◽  
Anders Meibom ◽  
...  
Keyword(s):  
Nutrient Limitation ◽  
Phenotypic Heterogeneity ◽  
Fluctuating Environments

scholarly journals On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation

2022 ◽  
Author(s):  
Monika Opalek ◽  
Bogna Smug ◽  
Michael Doebeli ◽  
Dominika Wloch-Salamon
Keyword(s):  
Phenotypic Heterogeneity ◽  
Microbial Populations ◽  
Cell Heterogeneity ◽  
Ecological Significance

Nongenetic cell heterogeneity is present in glucose-starved yeast populations in the form of quiescent (Q) and nonquiescent (NQ) phenotypes. There is evidence that Q cells help the population survive long starvation.

scholarly journals Quantitation and Comparison of Phenotypic Heterogeneity Among Single Cells of Monoclonal Microbial Populations

2019 ◽  
Vol 10 ◽  
Author(s):  
Federica Calabrese ◽  
Iryna Voloshynovska ◽  
Florin Musat ◽  
Martin Thullner ◽  
Michael Schlömann ◽  
...  
Keyword(s):  
Single Cells ◽  
Phenotypic Heterogeneity ◽  
Microbial Populations

scholarly journals Phenotypic heterogeneity is adaptive for microbial populations under starvation

2021 ◽  
Author(s):  
Monika Opalek ◽  
Bogna Smug ◽  
Michael Doebeli ◽  
Dominika Magdalena Wloch-Salamon
Keyword(s):  
Nutrient Recycling ◽  
Phenotypic Heterogeneity ◽  
Microbial Populations ◽  
Lag Phase ◽  
Starvation Period ◽  
Quiescent State ◽  
Bet Hedging ◽  
Quiescent Cells ◽  
Variable Environments ◽  
Over Time

To persist in variable environments populations of microorganisms have to survive periods of starvation and be able to restart cell division in nutrient-rich conditions. Typically, starvation signals initiate a transition to a quiescent state in a fraction of individual cells, while the rest of the cells remain non-quiescent. It is widely believed that, while quiescent cells (Q) help the population to survive long starvation, the non-quiescent cells (NQ) are a side effect of imperfect transition. We analysed regrowth of starved monocultures of Q and NQ cells compared to mixed, heterogeneous cultures in simple and complex starvation environments. Our experiments, as well as mathematical modelling, demonstrate that Q monocultures benefit from better survival during long starvation, and from a shorter lag phase after resupply of rich medium. However, when the starvation period is very short, the NQ monocultures outperform Q and mixed cultures, due to their short lag phase. In addition, only NQ monocultures benefit from complex starvation environments, where nutrient recycling is possible. Our study suggests that phenotypic heterogeneity in starved populations could be a form of bet hedging, which is adaptive when environmental determinants, such as the length of the starvation period, the length of the regrowth phase, and the complexity of the starvation environment vary over time.

scholarly journals Ecological feedback in quorum-sensing microbial populations can induce heterogeneous production of autoinducers

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Matthias Bauer ◽  
Johannes Knebel ◽  
Matthias Lechner ◽  
Peter Pickl ◽  
Erwin Frey
Keyword(s):  
Gene Expression ◽  
Quorum Sensing ◽  
Promoter Activity ◽  
Phenotypic Heterogeneity ◽  
Microbial Populations ◽  
Alternative Mechanism ◽  
Stochastic Gene Expression ◽  
Regulatory Circuits ◽  
Gene Regulatory ◽  
Gene Regulatory Circuits

Autoinducers are small signaling molecules that mediate intercellular communication in microbial populations and trigger coordinated gene expression via ‘quorum sensing’. Elucidating the mechanisms that control autoinducer production is, thus, pertinent to understanding collective microbial behavior, such as virulence and bioluminescence. Recent experiments have shown a heterogeneous promoter activity of autoinducer synthase genes, suggesting that some of the isogenic cells in a population might produce autoinducers, whereas others might not. However, the mechanism underlying this phenotypic heterogeneity in quorum-sensing microbial populations has remained elusive. In our theoretical model, cells synthesize and secrete autoinducers into the environment, up-regulate their production in this self-shaped environment, and non-producers replicate faster than producers. We show that the coupling between ecological and population dynamics through quorum sensing can induce phenotypic heterogeneity in microbial populations, suggesting an alternative mechanism to stochastic gene expression in bistable gene regulatory circuits.

scholarly journals Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus Sulfurovum in Geographically Distinct Deep-Sea Hydrothermal Vents

mSystems ◽  
2020 ◽  
Vol 5 (2) ◽  
Author(s):  
Alief Moulana ◽  
Rika E. Anderson ◽  
Caroline S. Fortunato ◽  
Julie A. Huber
Keyword(s):  
Natural Selection ◽  
Nutrient Limitation ◽  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Gene Content ◽  
Microbial Populations ◽  
Gene Gain ◽  
Microbial Genomes ◽  
Gain And Loss

ABSTRACT Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution. IMPORTANCE Microbes can alter their gene content through the gain and loss of genes. However, there is some debate as to whether natural selection or neutral processes play a stronger role in molding the gene content of microbial genomes. In this study, we examined variation in gene content for the Epsilonbacteraeota genus Sulfurovum from deep-sea hydrothermal vents, which are dynamic habitats known for extensive horizontal gene transfer within microbial populations. Our results show that natural selection is a strong driver of Sulfurovum gene content and that nutrient limitation in particular has shaped the Sulfurovum genome, leading to differences in gene content between ocean basins. Our results also suggest that recently acquired genes undergo stronger selection than genes that were acquired in the more distant past. Overall, our results highlight the importance of natural selection in driving the evolution of microbial populations in these dynamic habitats.

scholarly journals Phenotypic heterogeneity implements a game theoretic mixed strategy in a clonal microbial population

2014 ◽  
Author(s):  
David Healey ◽  
Jeff Gore
Keyword(s):  
Experimental Evidence ◽  
Evolutionary Game ◽  
Phenotypic Heterogeneity ◽  
Microbial Populations ◽  
Bet Hedging ◽  
Hedging Strategy ◽  
Unpredictable Environments ◽  
Game Theoretic ◽  
Pure Strategies ◽  
Genetic Mutants

Genetically identical cells in microbial populations often exhibit a remarkable degree of phenotypic heterogeneity even in homogenous environments. While such heterogeneity is often thought to be a bet-hedging strategy against unpredictable environments, evolutionary game theory also predicts phenotypic heterogeneity as a stable response to evolutionary "hawk-dove" games, in which rare strategies are favored over common ones. Here we provide experimental evidence for this game theoretic explanation in the context of the well-studied yeast GAL network. In an environment containing the two sugars glucose and galactose, the yeast GAL network displays stochastic bimodal activation. We show that genetic mutants playing the "pure" strategies of GAL-ON or GAL-OFF can each invade the opposite strategy when rare, indicating a hawk-dove game between the two. Consistent with the Nash equilibrium of an evolutionary game, the stable mix of pure strategists does not necessarily maximize the growth of the overall population. We also find that the wild type GAL network can invade populations of both pure strategists while remaining uninvasible by either. Taken together, our results provide experimental evidence that evolutionary hawk-dove games between identical cells can explain the phenotypic heterogeneity found in clonal microbial populations.

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