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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.