Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia
Abstract Background Cyclic di-guanylate (c-di-GMP), synthesized by diguanylate cyclase, is a major second messenger in prokaryotes, where it triggers biofilm formation. The dictyostelid social amoebas acquired diguanylate cyclase (dgcA) by horizontal gene transfer. Dictyostelium discoideum (Ddis) in...
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BMC
2023-10-01
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| Series: | BMC Ecology and Evolution |
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| Online Access: | https://doi.org/10.1186/s12862-023-02169-z |
| _version_ | 1797578567476838400 |
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| author | Yoshinori Kawabe Qingyou Du Takaaki B. Narita Craig Bell Christina Schilde Koryu Kin Pauline Schaap |
| author_facet | Yoshinori Kawabe Qingyou Du Takaaki B. Narita Craig Bell Christina Schilde Koryu Kin Pauline Schaap |
| author_sort | Yoshinori Kawabe |
| collection | DOAJ |
| description | Abstract Background Cyclic di-guanylate (c-di-GMP), synthesized by diguanylate cyclase, is a major second messenger in prokaryotes, where it triggers biofilm formation. The dictyostelid social amoebas acquired diguanylate cyclase (dgcA) by horizontal gene transfer. Dictyostelium discoideum (Ddis) in taxon group 4 uses c-di-GMP as a secreted signal to induce differentiation of stalk cells, the ancestral somatic cell type that supports the propagating spores. We here investigated how this role for c-di-GMP evolved in Dictyostelia by exploring dgcA function in the group 2 species Polysphondylium pallidum (Ppal) and in Polysphondylium violaceum (Pvio), which resides in a small sister clade to group 4. Results Similar to Ddis, dgcA is upregulated after aggregation in Ppal and Pvio and predominantly expressed in the anterior region and stalks of emerging fruiting bodies. DgcA null mutants in Ppal and Pvio made fruiting bodies with very long and thin stalks and only few spores and showed delayed aggregation and larger aggregates, respectively. Ddis dgcAˉ cells cannot form stalks at all, but showed no aggregation defects. The long, thin stalks of Ppal and Pvio dgcAˉ mutants were also observed in acaAˉ mutants in these species. AcaA encodes adenylate cyclase A, which mediates the effects of c-di-GMP on stalk induction in Ddis. Other factors that promote stalk formation in Ddis are DIF-1, produced by the polyketide synthase StlB, low ammonia, facilitated by the ammonia transporter AmtC, and high oxygen, detected by the oxygen sensor PhyA (prolyl 4-hydroxylase). We deleted the single stlB, amtC and phyA genes in Pvio wild-type and dgcAˉ cells. Neither of these interventions affected stalk formation in Pvio wild-type and not or very mildly exacerbated the long thin stalk phenotype of Pvio dgcAˉ cells. Conclusions The study reveals a novel role for c-di-GMP in aggregation, while the reduced spore number in Pvio and Ppal dgcAˉ is likely an indirect effect, due to depletion of the cell pool by the extended stalk formation. The results indicate that in addition to c-di-GMP, Dictyostelia ancestrally used an as yet unknown factor for induction of stalk formation. The activation of AcaA by c-di-GMP is likely conserved throughout Dictyostelia. |
| first_indexed | 2024-03-10T22:24:38Z |
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| id | doaj.art-e4dced09f7fc4b9587c085a976b9adeb |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-03-10T22:24:38Z |
| publishDate | 2023-10-01 |
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| series | BMC Ecology and Evolution |
| spelling | doaj.art-e4dced09f7fc4b9587c085a976b9adeb2023-11-19T12:10:49ZengBMCBMC Ecology and Evolution2730-71822023-10-0123111410.1186/s12862-023-02169-zEmerging roles for diguanylate cyclase during the evolution of soma in dictyosteliaYoshinori Kawabe0Qingyou Du1Takaaki B. Narita2Craig Bell3Christina Schilde4Koryu Kin5Pauline Schaap6Molecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeMolecular Cell and Developmental Biology, School of Life Sciences, University of DundeeAbstract Background Cyclic di-guanylate (c-di-GMP), synthesized by diguanylate cyclase, is a major second messenger in prokaryotes, where it triggers biofilm formation. The dictyostelid social amoebas acquired diguanylate cyclase (dgcA) by horizontal gene transfer. Dictyostelium discoideum (Ddis) in taxon group 4 uses c-di-GMP as a secreted signal to induce differentiation of stalk cells, the ancestral somatic cell type that supports the propagating spores. We here investigated how this role for c-di-GMP evolved in Dictyostelia by exploring dgcA function in the group 2 species Polysphondylium pallidum (Ppal) and in Polysphondylium violaceum (Pvio), which resides in a small sister clade to group 4. Results Similar to Ddis, dgcA is upregulated after aggregation in Ppal and Pvio and predominantly expressed in the anterior region and stalks of emerging fruiting bodies. DgcA null mutants in Ppal and Pvio made fruiting bodies with very long and thin stalks and only few spores and showed delayed aggregation and larger aggregates, respectively. Ddis dgcAˉ cells cannot form stalks at all, but showed no aggregation defects. The long, thin stalks of Ppal and Pvio dgcAˉ mutants were also observed in acaAˉ mutants in these species. AcaA encodes adenylate cyclase A, which mediates the effects of c-di-GMP on stalk induction in Ddis. Other factors that promote stalk formation in Ddis are DIF-1, produced by the polyketide synthase StlB, low ammonia, facilitated by the ammonia transporter AmtC, and high oxygen, detected by the oxygen sensor PhyA (prolyl 4-hydroxylase). We deleted the single stlB, amtC and phyA genes in Pvio wild-type and dgcAˉ cells. Neither of these interventions affected stalk formation in Pvio wild-type and not or very mildly exacerbated the long thin stalk phenotype of Pvio dgcAˉ cells. Conclusions The study reveals a novel role for c-di-GMP in aggregation, while the reduced spore number in Pvio and Ppal dgcAˉ is likely an indirect effect, due to depletion of the cell pool by the extended stalk formation. The results indicate that in addition to c-di-GMP, Dictyostelia ancestrally used an as yet unknown factor for induction of stalk formation. The activation of AcaA by c-di-GMP is likely conserved throughout Dictyostelia.https://doi.org/10.1186/s12862-023-02169-zDictyostelid social amoebasEvolution of somaDiguanylate cyclaseAdenylate cyclase Aammonia transporter CProlyl 4-hydroxylase |
| spellingShingle | Yoshinori Kawabe Qingyou Du Takaaki B. Narita Craig Bell Christina Schilde Koryu Kin Pauline Schaap Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia BMC Ecology and Evolution Dictyostelid social amoebas Evolution of soma Diguanylate cyclase Adenylate cyclase A ammonia transporter C Prolyl 4-hydroxylase |
| title | Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| title_full | Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| title_fullStr | Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| title_full_unstemmed | Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| title_short | Emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| title_sort | emerging roles for diguanylate cyclase during the evolution of soma in dictyostelia |
| topic | Dictyostelid social amoebas Evolution of soma Diguanylate cyclase Adenylate cyclase A ammonia transporter C Prolyl 4-hydroxylase |
| url | https://doi.org/10.1186/s12862-023-02169-z |
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