Details
| Original language | English |
|---|---|
| Article number | 2524 |
| Journal | Frontiers in microbiology |
| Volume | 9 |
| Issue number | OCT |
| Publication status | Published - 23 Oct 2018 |
| Externally published | Yes |
Abstract
To proliferate, antibiotic-producing Streptomyces undergo a complex developmental transition from vegetative growth to the production of aerial hyphae and spores. This morphological switch is controlled by the signaling molecule cyclic bis-(3',5') di-guanosine-mono-phosphate (c-di-GMP) that binds to the master developmental regulator, BldD, leading to repression of key sporulation genes during vegetative growth. However, a systematical analysis of all the GGDEF/EAL/HD-GYP proteins that control c-di-GMP levels in Streptomyces is still lacking. Here, we have FLAG-tagged all 10 c-di-GMP turnover proteins in Streptomyces venezuelae and characterized their expression patterns throughout the life cycle, revealing that the diguanylate cyclase (DGC) CdgB and the phosphodiesterase (PDE) RmdB are the most abundant GGDEF/EAL proteins. Moreover, we have deleted all the genes coding for c-di-GMP turnover enzymes individually and analyzed morphogenesis of the mutants in macrocolonies. We show that the composite GGDEF-EAL protein CdgC is an active DGC and that deletion of the DGCs cdgB and cdgC enhance sporulation whereas deletion of the PDEs rmdA and rmdB delay development in S. venezuelae. By comparing the pan genome of 93 fully sequenced Streptomyces species we show that the DGCs CdgA, CdgB, and CdgC, and the PDE RmdB represent the most conserved c-di-GMP-signaling proteins in the genus Streptomyces.
Keywords
- C-di-GMP, Development, EAL, GGDEF, HD-GYP, Streptomyces
ASJC Scopus subject areas
- Immunology and Microbiology(all)
- Microbiology
- Medicine(all)
- Microbiology (medical)
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In: Frontiers in microbiology, Vol. 9, No. OCT, 2524, 23.10.2018.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
T1 - Expression Patterns, Genomic Conservation and Input Into Developmental Regulation of the GGDEF/EAL/HD-GYP Domain Proteins in Streptomyces
AU - Al-Bassam, Mahmoud M
AU - Haist, Julian
AU - Neumann, Sara Alina
AU - Lindenberg, Sandra
AU - Tschowri, Natalia
N1 - Funding information: We are grateful to Ann-Brit Johanna Klatt for generation of the cSVAK-2 cosmid and the SVABK-4 strain and to Jakob Müller for construction of the pSVOJ1 plasmid. We thank Mark Buttner for reading the manuscript and providing constructive comments. We also acknowledge support by the German Research Foundation (DFG) and the Open Access Publication Fund of Humboldt-Universität zu Berlin. This work was supported by the German Research Foundation (DFG) Emmy Noether program and a priority program SPP1879 grant to NT (TS 325/1-1 and TS 325/2-1).
PY - 2018/10/23
Y1 - 2018/10/23
N2 - To proliferate, antibiotic-producing Streptomyces undergo a complex developmental transition from vegetative growth to the production of aerial hyphae and spores. This morphological switch is controlled by the signaling molecule cyclic bis-(3',5') di-guanosine-mono-phosphate (c-di-GMP) that binds to the master developmental regulator, BldD, leading to repression of key sporulation genes during vegetative growth. However, a systematical analysis of all the GGDEF/EAL/HD-GYP proteins that control c-di-GMP levels in Streptomyces is still lacking. Here, we have FLAG-tagged all 10 c-di-GMP turnover proteins in Streptomyces venezuelae and characterized their expression patterns throughout the life cycle, revealing that the diguanylate cyclase (DGC) CdgB and the phosphodiesterase (PDE) RmdB are the most abundant GGDEF/EAL proteins. Moreover, we have deleted all the genes coding for c-di-GMP turnover enzymes individually and analyzed morphogenesis of the mutants in macrocolonies. We show that the composite GGDEF-EAL protein CdgC is an active DGC and that deletion of the DGCs cdgB and cdgC enhance sporulation whereas deletion of the PDEs rmdA and rmdB delay development in S. venezuelae. By comparing the pan genome of 93 fully sequenced Streptomyces species we show that the DGCs CdgA, CdgB, and CdgC, and the PDE RmdB represent the most conserved c-di-GMP-signaling proteins in the genus Streptomyces.
AB - To proliferate, antibiotic-producing Streptomyces undergo a complex developmental transition from vegetative growth to the production of aerial hyphae and spores. This morphological switch is controlled by the signaling molecule cyclic bis-(3',5') di-guanosine-mono-phosphate (c-di-GMP) that binds to the master developmental regulator, BldD, leading to repression of key sporulation genes during vegetative growth. However, a systematical analysis of all the GGDEF/EAL/HD-GYP proteins that control c-di-GMP levels in Streptomyces is still lacking. Here, we have FLAG-tagged all 10 c-di-GMP turnover proteins in Streptomyces venezuelae and characterized their expression patterns throughout the life cycle, revealing that the diguanylate cyclase (DGC) CdgB and the phosphodiesterase (PDE) RmdB are the most abundant GGDEF/EAL proteins. Moreover, we have deleted all the genes coding for c-di-GMP turnover enzymes individually and analyzed morphogenesis of the mutants in macrocolonies. We show that the composite GGDEF-EAL protein CdgC is an active DGC and that deletion of the DGCs cdgB and cdgC enhance sporulation whereas deletion of the PDEs rmdA and rmdB delay development in S. venezuelae. By comparing the pan genome of 93 fully sequenced Streptomyces species we show that the DGCs CdgA, CdgB, and CdgC, and the PDE RmdB represent the most conserved c-di-GMP-signaling proteins in the genus Streptomyces.
KW - C-di-GMP
KW - Development
KW - EAL
KW - GGDEF
KW - HD-GYP
KW - Streptomyces
UR - http://www.scopus.com/inward/record.url?scp=85055825274&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2018.02524
DO - 10.3389/fmicb.2018.02524
M3 - Article
C2 - 30405580
VL - 9
JO - Frontiers in microbiology
JF - Frontiers in microbiology
SN - 1664-302X
IS - OCT
M1 - 2524
ER -