On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation
ABSTRACT 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 re...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00450-21 |
| _version_ | 1819279607121051648 |
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| author | Monika Opalek Bogna Smug Michael Doebeli Dominika Wloch-Salamon |
| author_facet | Monika Opalek Bogna Smug Michael Doebeli Dominika Wloch-Salamon |
| author_sort | Monika Opalek |
| collection | DOAJ |
| description | ABSTRACT 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. IMPORTANCE 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. |
| first_indexed | 2024-12-24T00:30:35Z |
| format | Article |
| id | doaj.art-a4e589aaba144470a94fa627e14df657 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-24T00:30:35Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-a4e589aaba144470a94fa627e14df6572022-12-21T17:24:16ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-02-0110110.1128/spectrum.00450-21On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing StarvationMonika Opalek0Bogna Smug1Michael Doebeli2Dominika Wloch-Salamon3Jagiellonian University, Faculty of Biology, Institute of Environmental Sciences, Kraków, PolandMalopolska Centre of Biotechnology, Jagiellonian University, Kraków, PolandDepartment of Zoology, University of British Columbia, British Columbia, Vancouver, CanadaJagiellonian University, Faculty of Biology, Institute of Environmental Sciences, Kraków, PolandABSTRACT 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. IMPORTANCE 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.https://journals.asm.org/doi/10.1128/spectrum.00450-21S. cerevisiaebet hedgingevolutionary biologymathematical modellingquiescencestarvation |
| spellingShingle | Monika Opalek Bogna Smug Michael Doebeli Dominika Wloch-Salamon On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation Microbiology Spectrum S. cerevisiae bet hedging evolutionary biology mathematical modelling quiescence starvation |
| title | On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation |
| title_full | On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation |
| title_fullStr | On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation |
| title_full_unstemmed | On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation |
| title_short | On the Ecological Significance of Phenotypic Heterogeneity in Microbial Populations Undergoing Starvation |
| title_sort | on the ecological significance of phenotypic heterogeneity in microbial populations undergoing starvation |
| topic | S. cerevisiae bet hedging evolutionary biology mathematical modelling quiescence starvation |
| url | https://journals.asm.org/doi/10.1128/spectrum.00450-21 |
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