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MBE Advance Access published online on July 17, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn156
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© 2008 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

From Drought Sensing to Developmental Control: Evolution of Cyclic AMP Signaling in Social Amoebas

Allyson V. Ritchie1, Saskia van Es2, Celine Fouquet3 and Pauline Schaap*

School of Life Sciences, University of Dundee, UK
1 Department of Haematology, University of Cambridge, Cambridge CB 2PT, UK
2 Earth and Life Sciences, Free University of Amsterdam, 1081 HV Amsterdam, The Netherlands
3 LPPA UMR7152 Collège de France, 75005 Paris, France

* Corresponding author, Pauline Schaap, MSI/WTB/JBC complex, Dow Street, Dundee, DD1 5EH, UK, Phone: 44 1382 388078; Fax: 44 1382 345386, E-mail: p.schaap{at}dundee.ac.uk

Received for publication May 25, 2008. Revision received July 2, 2008. Accepted for publication July 12, 2008.

Amoebas and other protists commonly encyst when faced with environmental stress. While little is known of the signalling pathways that mediate encystation, the analogous process of spore formation in Dictyostelid social amoebas is better understood. In Dictyostelium discoideum, secreted cyclic AMP (cAMP) mediates the aggregation of starving amoebas and induces the differentiation of prespore cells. Intracellular cAMP acting on cAMP-dependent protein kinase (PKA) triggers the maturation of spores and prevents their germination under the prevalent conditions of high osmolality in the spore head. The osmolyte-activated adenylate cyclase, ACG, produces cAMP for prespore differentiation and inhibition of spore germination. To retrace the origin of ACG function, we investigated ACG gene conservation and function in species that span the dictyostelid phylogeny. ACG genes, osmolyte-activated ACG activity and osmo-regulation of spore germination were detected in species that represent the four major groups of Dictyostelia. Unlike the derived species D.discoideum, basal Dictyostelia have retained the ancestral mechanism of encystation from solitary amoebas. In these species and in solitary amoebas, encystation is independently triggered by starvation or by high osmolality. Osmolyte-induced encystation was accompanied by an increase in cAMP and prevented by inhibition of PKA, indicating that ACG and PKA activation mediate this response. We propose that high osmolality signals drought in soil amoebas and that developmental cAMP signaling in the Dictyostelia has evolved from this stress response.

Key Words: evolution of multicellularity • osmotic stress signalling • adenylate cyclase G • cell-type specialization • sporulation • encystation • drought sensing


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Y. Kawabe, T. Morio, J. L. James, A. R. Prescott, Y. Tanaka, and P. Schaap
Activated cAMP receptors switch encystation into sporulation
PNAS, April 28, 2009; 106(17): 7089 - 7094.
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