Publikationsserver der Universitätsbibliothek Marburg
Titel:Roles of the second messenger cyclic di-GMP in environmental adaptation of Sinorhizobium meliloti
Autor:Schäper, Simon
Weitere Beteiligte: Becker, Anke (Prof. Dr.)
Veröffentlicht:2017
URI:https://archiv.ub.uni-marburg.de/diss/z2017/0677
DOI: https://doi.org/10.17192/z2017.0677
URN: urn:nbn:de:hebis:04-z2017-06779
DDC:570 Biowissenschaften, Biologie
Titel (trans.):Funktionen des sekundären Botenstoffs zyklisches di-GMP in der Anpassung an die Umwelt von Sinorhizobium meliloti
Publikationsdatum:2019-11-05
Lizenz:https://creativecommons.org/licenses/by-sa/4.0

Dokument

Schlagwörter:

Summary:
Bacteria have evolved various systems for the integration of environmental signals to rapidly coordinate cellular pathways and adapt to changes in their environment. In the quickly advancing field of nucleotide-based second messengers, cyclic dimeric guanosine monophosphate (c-di-GMP) has emerged as a key regulatory player whose underlying signaling networks control major adaptational and lifestyle changes. Enzymes that catalyze synthesis and degradation of c-di-GMP, named diguanylate cylases (DGCs) and phosphodiesterases (PDEs), respectively, are near-ubiquitous in the bacterial kingdom. Despite the numerous studies aiming to better understand the role of c-di-GMP in bacteria, knowledge on integration of c-di-GMP networks into other regulatory networks, the molecular inventory of c-di-GMP receptors and molecular mechanisms underlying c-di-GMP-dependent regulation is limited. This study investigated roles of c-di-GMP in environmental adaptation of soil-dwelling Sinorhizobium meliloti, a rod-shaped alphaproteobacterium from the order Rhizobiales that exists either in free-living states or in symbiosis with leguminous plant hosts. The S. meliloti genome encodes 22 proteins putatively involved in synthesis, degradation and binding of c-di-GMP. Single mutations in 21 of these genes did not cause evident changes in surface attachment, swimming motility or exopolysaccharide (EPS) production. Moreover, screening the different phenotypes of S. meliloti c-di-GMP0 mutants revealed no defects in cell viability and symbiotic potency. In contrast, artificially increasing c-di-GMP levels by overproduction of several DGCs promoted production of extracellular matrix components and surface attachment, whereas swimming motility and extracellular accumulation of N-Acyl-homoserine lactones (AHLs) was reduced. The identification of genetic determinants responsible for observed phenotypic changes at elevated c-di-GMP levels proved c-di-GMP-dependent regulation at both transcriptional and post-translational levels. The SMc01790-SMc01796 locus, homologous to the Agrobacterium tumefaciens uppABCDEF cluster governing biosynthesis of a unipolar polysaccharide (UPP), was required for c-di-GMP-stimulated surface attachment, while the stand-alone PilZ domain protein SMc00507 (renamed McrA) acted as c-di-GMP receptor protein involved in regulation of swimming motility. Transcriptome profiling of S. meliloti at elevated c-di-GMP levels revealed upregulation of the uxs1-SMb20463 gene cluster governing biosynthesis of an extracellular polysaccharide (referred to as CUP). Resulting from this finding, AraC-like transcriptional activator SMb20457 (renamed CuxR) was shown to bind c-di-GMP by a mechanism similar to that of PilZ domains, which provided an example of convergent evolution in two distinct protein families. This study demonstrates that the c-di-GMP network in S. meliloti is integrated into other cellular systems, particularly the well-characterized regulatory network for opposing control of EPS biosynthesis and motility. For instance, CuxR-mediated activation of CUP production was counteracted by the global repressor MucR, while both MucR and the AHL-sensitive master regulator ExpR reduced UPP-mediated surface attachment at elevated c-di-GMP levels. Moreover, a new cellular function was assigned to the essential PDE SMc00074 (renamed GdcP), which is linked to cell envelope biogenesis in alpha-rhizobial species. Overall, c-di-GMP-dependent regulation of multiple cellular functions indicated that high c-di-GMP levels favor a sedentary lifestyle of free-living S. meliloti. The switch of single motile bacteria from a planktonic state to a structured community of cells might contribute to environmental adaptation and long-term survival of S. meliloti in its natural soil habitat.

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