Role of epigenetics in unicellular to multicellular transition in Dictyostelium

Simon Yuan Wang,Eric Lieberman Greer,George Sabin,Elizabeth Ann Pollina,Benjamin Aaron Garcia,Henry L Bushnell,I-Hao Wang,Lindsay Kristina Pino,Ken Takashima,Colette Fritsche,Paul Lieberman Greer

doi:10.1186/s13059-021-02360-9

Abstract

BackgroundThe evolution of multicellularity is a critical event that remains incompletely understood. We use the social amoeba, Dictyostelium discoideum, one of the rare organisms that readily transits back and forth between both unicellular and multicellular stages, to examine the role of epigenetics in regulating multicellularity.ResultsWhile transitioning to multicellular states, patterns of H3K4 methylation and H3K27 acetylation significantly change. By combining transcriptomics, epigenomics, chromatin accessibility, and orthologous gene analyses with other unicellular and multicellular organisms, we identify 52 conserved genes, which are specifically accessible and expressed during multicellular states. We validated that four of these genes, including the H3K27 deacetylase hdaD, are necessary and that an SMC-like gene, smcl1, is sufficient for multicellularity in Dictyostelium.ConclusionsThese results highlight the importance of epigenetics in reorganizing chromatin architecture to facilitate multicellularity in Dictyostelium discoideum and raise exciting possibilities about the role of epigenetics in the evolution of multicellularity more broadly.

Highlights

The evolution of multicellularity is a critical event that remains incompletely understood
Dictyostelium display unicellular and multicellular specific chromatin patterns To begin to determine whether chromatin modifications might contribute to D. discoideum life cycle changes, overall histone methylation and acetylation levels were assessed by western blots at different cellularity stages
These analyses revealed that histone H3 lysine 4 trimethylation (H3K4me3) levels decreased and H3K4me1 increased significantly upon the transition to multicellularity suggesting that chromatin modification might help regulate the transition to multicellularity in Dictyostelium (Additional file 1: Figure S1A)

Summary

Introduction

The evolution of multicellularity is a critical event that remains incompletely understood. Multicellularity is believed to have evolved due to both aggregation of non-clonal single cells cooperating to form a multicellular organism [2] and to clonal development where the individual cells never dissociate [3, 4]. How this evolution from primitive amoeba or fungal unicellular organisms occurred ~ 900 million years ago is still incompletely understood [5]. The acquisition of new transcription factor networks does not always correlate with multicellularity [9] These observations suggest a potential role for chromatin regulation in the transition to multicellularity. Whether the increased complexity of epigenetic regulation may have helped to drive the transition to multicellularity is unknown

Methods

Results

Conclusion