Jagiellonian University, Faculty of Biology, Institute of Environmental Sciences, Kraków, Poland.
Malopolska Centre of Biotechnology, Jagiellonian University, Kraków, Poland.
Microbiol Spectr. 2022 Feb 23;10(1):e0045021. doi: 10.1128/spectrum.00450-21. Epub 2022 Jan 12.
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 nonquiescent. It is widely believed that, while quiescent (Q) cells help the population to survive long starvation, the nonquiescent (NQ) cells are a side effect of imperfect transition. We analyzed the regrowth of starved monocultures of Q and NQ cells compared to that of mixed, heterogeneous cultures from simple and complex starvation environments. Our experiments, as well as mathematical modeling, 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 that 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. 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. However, the role of the NQ cell type is not known, and it has been speculated that the NQ phenotype is just a side effect of the imperfect transition to the Q phenotype. Here, we show that, in contrast, there are ecological scenarios in which NQ cells perform better than monocultures of Q cells or naturally occurring mixed populations containing both Q and NQ cells. NQ cells benefit when the starvation period is very short and environmental conditions allow nutrient recycling during starvation. Our experimental and mathematical modeling results suggest a novel hypothesis: the presence of both Q and NQ phenotypes within starved yeast populations may reflect a form of bet hedging where different phenotypes provide fitness advantages depending on the environmental conditions.
为了在多变的环境中生存，微生物种群必须能够在饥饿时期存活，并在富含营养的条件下重新开始细胞分裂。通常情况下，饥饿信号会引发部分细胞进入休眠状态，而其余细胞则保持非休眠状态。人们普遍认为，虽然休眠（Q）细胞有助于种群在长时间的饥饿中存活，但非休眠（NQ）细胞是过渡不完美的副作用。我们分析了饥饿的 Q 和 NQ 细胞的纯培养物与简单和复杂饥饿环境中的混合、异质培养物的再生长情况。我们的实验以及数学模型表明，在长时间的饥饿中，Q 纯培养物的生存能力更好，在富含营养的培养基再供应后，其滞后阶段更短。然而，当饥饿期非常短时，由于 NQ 纯培养物的滞后阶段较短，因此其表现优于 Q 纯培养物和混合培养物。此外，只有 NQ 纯培养物受益于可能存在营养物质再循环的复杂饥饿环境。我们的研究表明，在饥饿的种群中表现出的表型异质性可能是一种适应性的贝叶斯博弈，当环境决定因素（如饥饿期的长短、再生长阶段的长短以及饥饿环境的复杂性）随时间变化时，这种异质性是有利的。在葡萄糖饥饿的酵母种群中，存在以休眠（Q）和非休眠（NQ）表型形式存在的非遗传细胞异质性。有证据表明，Q 细胞有助于种群在长时间的饥饿中存活。然而，NQ 细胞类型的作用尚不清楚，有人推测 NQ 表型只是向 Q 表型过渡不完美的副作用。在这里，我们表明，相反，在一些生态场景中，NQ 细胞的表现要好于 Q 细胞的纯培养物或自然存在的同时含有 Q 和 NQ 细胞的混合种群。当饥饿期非常短并且在饥饿期间允许营养物质再循环时，NQ 细胞会受益。我们的实验和数学模型结果提出了一个新的假设：在饥饿的酵母种群中存在 Q 和 NQ 表型可能反映了一种贝叶斯博弈，其中不同的表型根据环境条件提供适应优势。
