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An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae

The social amoeba Dictyostelium discoideum is widely studied for its multicellular development program as a response to starvation. Aggregates of up to 10 (6) cells form fruiting bodies containing (i) dormant spores (~80%) that can persist for months in the absence of nutrients, and (ii) dead stalk...

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Autores principales: Dubravcic, Darja, van Baalen, Minus, Nizak, Clément
Formato: Online Artículo Texto
Lenguaje:English
Publicado: F1000Research 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4184345/
https://www.ncbi.nlm.nih.gov/pubmed/25309731
http://dx.doi.org/10.12688/f1000research.4218.2
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author Dubravcic, Darja
van Baalen, Minus
Nizak, Clément
author_facet Dubravcic, Darja
van Baalen, Minus
Nizak, Clément
author_sort Dubravcic, Darja
collection PubMed
description The social amoeba Dictyostelium discoideum is widely studied for its multicellular development program as a response to starvation. Aggregates of up to 10 (6) cells form fruiting bodies containing (i) dormant spores (~80%) that can persist for months in the absence of nutrients, and (ii) dead stalk cells (~20%) that promote the dispersion of the spores towards nutrient-rich areas. It is often overlooked that not all cells aggregate upon starvation. Using a new quantitative approach based on time-lapse fluorescence microscopy and a low ratio of reporting cells, we have quantified this fraction of non-aggregating cells. In realistic starvation conditions, up to 15% of cells do not aggregate, which makes this third cell fate a significant component of the population-level response of social amoebae to starvation. Non-aggregating cells have an advantage over cells in aggregates since they resume growth earlier upon arrival of new nutrients, but have a shorter lifespan under prolonged starvation. We find that phenotypic heterogeneities linked to cell nutritional state bias the representation of cells in the aggregating vs. non-aggregating fractions, and thus affect population partitioning. Next, we report that the fraction of non-aggregating cells depends on genetic factors that regulate the timing of starvation, signal sensing efficiency and aggregation efficiency. In addition, interactions between clones in mixtures of non-isogenic cells affect the partitioning of each clone into both fractions. We further build a numerical model to test the evolutionary significance of the non-aggregating cell fraction. The partitioning of cells into aggregating and non-aggregating fractions is optimal in fluctuating environments with an unpredictable duration of starvation periods. Our study highlights the unicellular component of the response of social amoebae to starvation, and thus extends its evolutionary and ecological framework.
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spelling pubmed-41843452014-10-09 An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae Dubravcic, Darja van Baalen, Minus Nizak, Clément F1000Res Research Article The social amoeba Dictyostelium discoideum is widely studied for its multicellular development program as a response to starvation. Aggregates of up to 10 (6) cells form fruiting bodies containing (i) dormant spores (~80%) that can persist for months in the absence of nutrients, and (ii) dead stalk cells (~20%) that promote the dispersion of the spores towards nutrient-rich areas. It is often overlooked that not all cells aggregate upon starvation. Using a new quantitative approach based on time-lapse fluorescence microscopy and a low ratio of reporting cells, we have quantified this fraction of non-aggregating cells. In realistic starvation conditions, up to 15% of cells do not aggregate, which makes this third cell fate a significant component of the population-level response of social amoebae to starvation. Non-aggregating cells have an advantage over cells in aggregates since they resume growth earlier upon arrival of new nutrients, but have a shorter lifespan under prolonged starvation. We find that phenotypic heterogeneities linked to cell nutritional state bias the representation of cells in the aggregating vs. non-aggregating fractions, and thus affect population partitioning. Next, we report that the fraction of non-aggregating cells depends on genetic factors that regulate the timing of starvation, signal sensing efficiency and aggregation efficiency. In addition, interactions between clones in mixtures of non-isogenic cells affect the partitioning of each clone into both fractions. We further build a numerical model to test the evolutionary significance of the non-aggregating cell fraction. The partitioning of cells into aggregating and non-aggregating fractions is optimal in fluctuating environments with an unpredictable duration of starvation periods. Our study highlights the unicellular component of the response of social amoebae to starvation, and thus extends its evolutionary and ecological framework. F1000Research 2014-12-05 /pmc/articles/PMC4184345/ /pubmed/25309731 http://dx.doi.org/10.12688/f1000research.4218.2 Text en Copyright: © 2014 Dubravcic D et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. http://creativecommons.org/publicdomain/zero/1.0/ Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).
spellingShingle Research Article
Dubravcic, Darja
van Baalen, Minus
Nizak, Clément
An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title_full An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title_fullStr An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title_full_unstemmed An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title_short An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae
title_sort evolutionarily significant unicellular strategy in response to starvation in dictyostelium social amoebae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4184345/
https://www.ncbi.nlm.nih.gov/pubmed/25309731
http://dx.doi.org/10.12688/f1000research.4218.2
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