Role of Potassium Uptake Systems in Sinorhizobium meliloti Osmoadaptation and Symbiotic Performance

Abstract

Stimulation of potassium uptake is the most rapid response to an osmotic upshock in bacteria. This cation accumulates by a number of different transport systems whose importance has not been previously addressed for rhizobia. In silico analyses reveal the presence of genes encoding four possible potassium uptake systems in the genome of Sinorhizobium meliloti 1021: Kup1, Kup2, Trk, and Kdp. The study of the relevance of these systems under a number of different growth conditions and in symbiosis showed that the integrity of Kup1 or Trk is essential for growth under laboratory conditions even in osmotically balanced media and the absence of both systems leads to a reduced infectivity and competitiveness of the bacteria in alfalfa roots. Trk is the main system involved in the accumulation of potassium after an osmotic upshift and the most important system for growth of S. meliloti under hyperosmotic conditions. The other three systems, especially Kup1, are also relevant during the osmotic adaptation of the cell, and the relative importance of the Kdp system increases at low potassium concentrations.Rhizobia are gram-negative soil bacteria able to establish nitrogen-fixing symbiosis with leguminous plants under conditions of nitrogen deprivation. During this process, an exchange of molecular signals occurs between the two partners, leading to the formation of the root nodule, where biological nitrogen fixation takes place (12).Nearly 40% of the world's land surface can be categorized as having potential salinity problems (38). Most crops are sensitive to relatively low levels of salinity (36), and in the case of legumes, there is an additional problem since not only the plant but also the symbiotic bacteria are sensitive to salinity both at the free-living stage and during the symbiotic process (22). The Rhizobium-legume symbiosis is highly sensitive to salt or osmotic stress, since these conditions may inhibit the initial steps of the symbiotic interaction (root colonization, nodule infection, and nodule development) and also have a depressive effect on nitrogen fixation (38). It has been observed that Rhizobium mutants affected in adaptation to high salinity present deficiencies in their symbiotic capacity (25). These results emphasize the importance of studying the mechanisms of rhizobial adaptation to changes in the osmotic conditions of the soil environment.Response and adaptation to environmental stresses probably constitute a complex phenomenon involving many physiological and biochemical processes that likely reflect changes in gene expression and in the activities of enzymes and transport proteins (6,7,23). A rise in the external salinity and osmolarity triggers the outflow of water from the cell, resulting in a reduction in turgor and dehydration of the cytoplasm, causing a decrease in the cytoplasm volume and thus an increase in the ion concentration in the cytosol (33). A recent transcriptomic study of Sinorhizobium meliloti has revealed that the responses of this bacterium to ionic and nonionic compoun...

Plasmids with a Chromosome-Like Role in Rhizobia

“…Transport functions include a kdpABCD operon, encoding one of the four predicted potassium uptake systems (14), as well as the actP and hmrR genes, involved in copper expulsion. A gene that might be involved in selenocysteinetRNA formation (selA) was also found.…”

Role for cis -Acting RNA Sequences in the Temperature-Dependent Expression of the Multiadhesive Lig Proteins in Leptospira interrogans

“…The L. interrogans genome encodes homologs of the Kdp and Trk-like Ktr potassium transporters (58,59). Disruption of genes encoding Trk, Ktr, and Kdp transporters attenuates growth of diverse bacteria during osmotic stress (60)(61)(62)(63)(64).…”

Importance of Trehalose Biosynthesis for Sinorhizobium meliloti Osmotolerance and Nodulation of Alfalfa Roots

“…During this process, an exchange of molecular signals occurs between the two partners, leading to the formation of the root nodule, where biological nitrogen fixation takes place (12). It has been observed that rhizobium mutants affected in adaptation to high salinity present deficiencies in their symbiotic capacity (27,7,25). These results emphasize the importance of studying the adaptation mechanisms of rhizobia to osmotically unbalanced environmental conditions.…”

“…Rhizobia may use distinct mechanisms in response to hyperosmotic conditions, such as stimulation of potassium uptake (7), changes in cell morphology and size, or modifications in the pattern of extracellular polysaccharides (18,35,42). Nevertheless, one of the most general responses for long-term adaptation to osmotic stress is the intracellular accumulation of osmoprotective compounds (24,45).…”