Abstract
In multicellular organisms, the specification, coordination, and compartmentalization of cell types enable the formation of complex body plans. However, some eukaryotic protists such as slime molds generate diverse and complex structures while remaining in a multinucleate syncytial state. It is unknown if different regions of these giant syncytial cells have distinct transcriptional responses to environmental encounters and if nuclei within the cell diversify into heterogeneous states. Here, we performed spatial transcriptome analysis of the slime mold Physarum polycephalum in the plasmodium state under different environmental conditions and used single-nucleus RNA-sequencing to dissect gene expression heterogeneity among nuclei. Our data identifies transcriptome regionality in the organism that associates with proliferation, syncytial substructures, and localized environmental conditions. Further, we find that nuclei are heterogenous in their transcriptional profile and may process local signals within the plasmodium to coordinate cell growth, metabolism, and reproduction. To understand how nuclei variation within the syncytium compares to heterogeneity in single-nucleus cells, we analyzed states in single Physarum amoebal cells. We observed amoebal cell states at different stages of mitosis and meiosis, and identified cytokinetic features that are specific to nuclei divisions within the syncytium. Notably, we do not find evidence for predefined transcriptomic states in the amoebae that are observed in the syncytium. Our data shows that a single-celled slime mold can control its gene expression in a region-specific manner while lacking cellular compartmentalization and suggests that nuclei are mobile processors facilitating local specialized functions. More broadly, slime molds offer the extraordinary opportunity to explore how organisms can evolve regulatory mechanisms to divide labor, specialize, balance competition with cooperation, and perform other foundational principles that govern the logic of life.
Highlights
Animals and other multicellular organisms are composed of diverse, compartmentalized cell types that perform specialized functions
Differences in nuclei sizes originate from the single imaging plane of the three-dimensional tubes of the plasmodium and rarely by contamination of the autofluorescence of larger vesicles. https://elifesciences.org/articles/69745/figures#video1 interlaced tubes of varying diameters, and it was recently shown that these tubes grow and shrink in diameter in response to a nutrient source, thereby functioning to imprint the nutrient’s location in the tube diameter hierarchy (Kramar and Alim, 2021)
Nuclei are distributed throughout the slime mold syncytium and can be mobile We pursued several whole-plasmodium imaging experiments on fixed and live plasmodial cultures to better understand nuclei size, location, and
Summary
Animals and other multicellular organisms are composed of diverse, compartmentalized cell types that perform specialized functions. The syncytium, a cytoplasmic mass containing numerous nuclei that store genetic material including deoxyribonucleic acid (DNA), originates either through merging of cells or through nuclear divisions lacking an accompanying cell division. An example for the latter mode of syncytia formation are the plasmodia of many slime molds, such as Physarum polycephalum. Such acellular slime molds are able to generate complex and dynamic body structures covering tens of centimeters or more while lacking compartmentalization of nuclei into discrete cellular units. The underlying molecular processes that lead to syncytium formation and enable different subdomains to respond to dynamic environments are poorly understood
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