Activated cAMP receptors switch encystation into sporulation

Area of Science:

• Cellular and Molecular Biology
• Developmental Biology
• Evolutionary Biology

Background:

• Metazoan embryogenesis relies on repetitive signaling modules.
• Social amoeba development also features reiterated use of cyclic adenosine monophosphate (cAMP) signaling.
• In Dictyostelium discoideum, cAMP coordinates aggregation, fruiting body formation, and gene expression via four cAMP receptors (cARs1-4).

Purpose of the Study:

• Investigate the hierarchy and function of cAMP receptors (cARs) across social amoeba phylogeny.
• Understand the evolutionary origins of cAMP signaling in social amoebas.
• Determine the specific roles of cARs in development and survival strategies.

Main Methods:

• Phylogenetic analysis of cAR genes in social amoebas.
• Gene disruption experiments in Polysphondylium pallidum (Ppal) to create cAR null mutants.
• Observation and analysis of aggregation, fruiting body morphogenesis, and gene expression in wild-type and mutant strains.

Main Results:

• Gene duplications yielding cARs 2-4 occurred late in evolution; many species possess only a cAR1 ortholog.
• Disruption of Ppal cAR genes did not affect aggregation but caused complete failure in fruiting body morphogenesis.
• Mutants failed to form spores, exhibiting a defect in cAMP-induced spore gene expression, while encystation remained possible.

Conclusions:

• cAMP signaling in social amoebas likely evolved from cAMP-mediated encystation in solitary amoebas.
• cAMP secretion in aggregates promotes sporulation over encystation and organizes fruiting body development.
• cAMP-mediated cell aggregation represents the most recent evolutionary innovation in social amoeba development.