Adenylyl Cyclase G, an Osmosensor Controlling Germination of Dictyostelium Spores

Es, Saskia van; Virdy, Kiran J.; Pitt, Geoffrey S.; Meima, Marcel E; Sands, Todd W.; Devreotes, Peter N.; Cotter, David A.; Schaap, Pauline

doi:10.1074/jbc.271.39.23623

Cited by 79 publications

(97 citation statements)

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“…In these organisms, adenylate cyclase is considered to function as a receptor or a sensor (2,38). Recently, the adenylate cyclase of Dictyostelium that is expressed in spores was shown to be involved in sensing extracellular osmolarity (48). It is strongly suggested that the CyaA-like adenylate cyclase of cyanobacteria functions as a receptor or sensor.…”

Section: Discussionmentioning

confidence: 99%

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

Katayama

Ohmori

1997

J Bacteriol

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Adenylate cyclase genes, designated cyaA, cyaB1, cyaB2, cyaC, and cyaD, were isolated from the filamentous cyanobacterium Anabaena sp. strain PCC 7120 by complementation of a strain of Escherichia coli defective for the presence of cya. These genes encoded polypeptides consisting of 735, 859, 860, 1,155, and 546 amino acid residues, respectively. Deduced amino acid sequences of the regions near the C-terminal ends of these cya genes were similar to those of catalytic domains of eukaryotic adenylate cyclases. The remaining part of each cya gene towards its N-terminal end showed a characteristic structure. CyaA had two putative membrane-spanning regions. Both CyaB1 and CyaB2 had regions that were very similar to the cyclic GMP (cGMP)-binding domain of cGMP-stimulated cGMP phosphodiesterase. CyaC consisted of four distinct domains forming sequentially from the N terminus: a response regulator-like domain, a histidine kinase-like domain, a response regulatorlike domain, and the catalytic domain of adenylate cyclase. CyaD contained the forkhead-associated domain in its N-terminal region. Expression of these genes was examined by reverse transcription-PCR. The transcript of cyaC was shown to be predominant in this cyanobacterium. The cellular cyclic AMP level in the disruptant of the cyaC mutant was much lower than that in the wild type.Cyclic AMP (cAMP) regulates various biological activities in both prokaryotes and eukaryotes. In prokaryotes, cAMP and cAMP receptor protein regulate gene expression (7). In eukaryotes, cAMP regulates enzyme activity (11), channel activity (42), and gene expression (34) via the cAMP-dependent protein kinase. In cyanobacteria, it has been reported that cellular cAMP content is affected by growth conditions (17,22), that cAMP concentration changes rapidly in response to light-off and light-on signals (37) or to a pH shift (36), and that cAMP interferes with the pattern formation of heterocysts (43). However, it is still unknown whether cAMP functions as an intracellular signal molecule in cyanobacteria.Recently, we isolated adenylate cyclase (cya) genes from the filamentous cyanobacteria Anabaena cylindrica (26) and Spirulina platensis (52). Regions near the C-terminal ends of the adenylate cyclases of both cyanobacteria showed significant structural similarity to the catalytic domain of the adenylate cyclase of eukaryotes but showed no homology to that of prokaryotes such as Escherichia coli. Furthermore, cyanobacterial adenylate cyclases appeared to be membrane oriented.To study the physiological functions of these adenylate cyclases, disruption or overexpression of cya genes is indispensable. Unfortunately, both A. cylindrica and S. platensis are not transformable, so they are not suitable for this purpose. In this study, we isolated cya genes from a transformable cyanobacterium, Anabaena sp. strain PCC 7120, and constructed mutants defective in cya genes. Some physiological properties of these mutants were determined. MATERIALS AND METHODSStrains and growth conditions. Anabaena sp. s...

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Section: Discussionmentioning

confidence: 99%

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

Katayama

Ohmori

1997

J Bacteriol

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“…As mentioned above, ACG is localized on the spore surface, where it is directly activated by its extracellular osmo-sensing domain (Van Es et al, 1996). High levels of ammonium phosphate are released during spore maturation.…”

Section: Camp Regulation Of Fruiting Body Formationmentioning

confidence: 96%

“…In the 1990s, it became clear that, in addition to extracellular cAMP, intracellular cAMP acting on PKA was also required for prespore differentiation and was, furthermore, essential for spore and stalk maturation and for the control of spore germination (Harwood et al, 1992;Hopper et al, 1993;Van Es et al, 1996). For stalk and spore maturation, cAMP is produced by adenylate cyclase R (ACR), whereas cAMP for induction of prespore differentiation and control of spore germination is produced by adenylate cyclase G (ACG) Van Es et al, 1996;Alvarez-Curto et al, 2007). ACR harbours seven transmembrane domains and is embedded in the nuclear membrane of prestalk cells Alvarez-Curto et al, 2007;Chen et al, 2011).…”

Section: Camp Regulation Of Fruiting Body Formationmentioning

confidence: 99%

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Evolutionary crossroads in developmental biology: Dictyostelium discoideum

Schaap

2011

Development

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SummaryDictyostelium discoideum belongs to a group of multicellular life forms that can also exist for long periods as single cells. This ability to shift between uni-and multicellularity makes the group ideal for studying the genetic changes that occurred at the crossroads between uni-and multicellular life. In this Primer, I discuss the mechanisms that control multicellular development in Dictyostelium discoideum and reconstruct how some of these mechanisms evolved from a stress response in the unicellular ancestor.Key words: Evolution of multicellularity, Social amoeba, Encystation, Sporulation, Dictyostelium IntroductionThe social amoebas, or Dictyostelia, are a group of organisms that become multicellular by aggregation and then proceed to build fruiting bodies that consist of stalk cells and spores (see Glossary, Box 1). This developmental cycle is a response to starvation, and involves both highly coordinated cell movement and a tightly controlled programme of cell differentiation. Social amoebas belong to the supergroup of Amoebozoa (see Glossary, Box 1), a sister group to the clade of Opisthokonts (see Glossary, Box 1), which contains the animals and fungi. All supergroups contain unicellular protist-like organisms (see Glossary, Box 1) and, in several groups, multicellular life forms have evolved independently (Minge et al., 2009).The Amoebozoa supergroup consists mainly of unicellular amoeba-like organisms that have a simple life cycle. The feeding amoeba or trophozoite turns into a dormant cyst when faced with food shortage, drought or other life-threatening circumstances (Cavalier-Smith et al., 2004). Several clades of Amoebozoa have given rise to protostelid-like organisms (see Glossary, Box 1), which form a very simple fruiting body (see Glossary, Box 1) that consists of a single spore that sits on a simple stalk made by the same cell (Shadwick et al., 2009). However, only the Dictyostelia are able to form multicellular fruiting bodies that contain up to a million cells (Fig. 1).There are ~120 known species of Dictyostelia and a molecular phylogeny has been constructed to reveal the order in which they evolved (Schaap et al., 2006). The phylogeny subdivides species into four major groups (Fig. 2), with the model social amoeba Dictyostelium discoideum belonging to the most recently diverged group 4. Many species in groups 1-3 can still encyst as single cells when conditions are unfavourable for aggregation. However, group 4 species have lost the ability to encyst. Strikingly, all group 4 species tested secrete cyclic adenosine monophosphate (cAMP) to act as a chemoattractant for aggregation. This is most unusual, because almost all other organisms only use cAMP inside the cell to transduce the effect of other secreted stimuli, such as hormones, mating factors and neurotransmitters. None of the species in groups 1-3 uses cAMP for aggregation; some use glorin, a modified dipeptide of glutamate and ornithine, whereas others use folic acid, pterin or other as yet unidentified chemoattractants (Schaap e...

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“…In the fruiting body, spores are kept dormant by high osmolality, which directly activates ACG. ACG then activates PKA, resulting in inhibition of spore germination (22). In cyst forming species, such as Ppal, encystation is triggered by high osmolality, a signal for approaching drought, and this response is also mediated by ACG acting on PKA (12).…”

Section: Sporulation and Encystation Share Common Signaling Requiremementioning

confidence: 99%

Activated cAMP receptors switch encystation into sporulation

Kawabe

Morio

James

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Metazoan embryogenesis is controlled by a limited number of signaling modules that are used repetitively at successive developmental stages. The development of social amoebas shows similar reiterated use of cAMP-mediated signaling. In the model Dictyostelium discoideum, secreted cAMP acting on 4 cAMP receptors (cARs1-4) coordinates cell movement during aggregation and fruiting body formation, and induces the expression of aggregation and sporulation genes at consecutive developmental stages. To identify hierarchy in the multiple roles of cAMP, we investigated cAR heterogeneity and function across the social amoeba phylogeny. The gene duplications that yielded cARs 2-4 occurred late in evolution. Many species have only a cAR1 ortholog that duplicated independently in the Polysphondylids and Acytostelids. Disruption of both cAR genes of Polysphondylium pallidum (Ppal) did not affect aggregation, but caused complete collapse of fruiting body morphogenesis. The stunted structures contained disorganized stalk cells, which supported a mass of cysts instead of spores; cAMP triggered spore gene expression in Ppal, but not in the cAR null mutant, explaining its sporulation defect. Encystation is the survival strategy of solitary amoebas, and lower taxa, like Ppal, can still encyst as single cells. Recent findings showed that intracellular cAMP accumulation suffices to trigger encystation, whereas it is a complementary requirement for sporulation. Combined, the data suggest that cAMP signaling in social amoebas evolved from cAMP-mediated encystation in solitary amoebas; cAMP secretion in aggregates prompted the starving cells to form spores and not cysts, and additionally organized fruiting body morphogenesis. cAMP-mediated aggregation was the most recent innovation.developmental signaling ͉ evolution of multicellularity ͉ Dictyostelia ͉ Amoebozoa

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Adenylyl Cyclase G, an Osmosensor Controlling Germination of Dictyostelium Spores

Cited by 79 publications

References 22 publications

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120

Evolutionary crossroads in developmental biology: Dictyostelium discoideum

Activated cAMP receptors switch encystation into sporulation

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