RT Journal Article
SR Electronic
T1 Nuclei are mobile processors enabling specialization in a gigantic single-celled syncytium
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2021.04.29.441915
DO 10.1101/2021.04.29.441915
A1 Tobias Gerber
A1 Cristina Loureiro
A1 Nico Schramma
A1 Siyu Chen
A1 Akanksha Jain
A1 Anne Weber
A1 Anne Weigert
A1 Malgorzata Santel
A1 Karen Alim
A1 Barbara Treutlein
A1 J. Gray Camp
YR 2021
UL http://biorxiv.org/content/early/2021/04/30/2021.04.29.441915.abstract
AB 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 multinucleated 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-nucleated 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.Competing Interest StatementThe authors have declared no competing interest.