Biosynthesis of compatible solutes in rhizobial strains isolated from Phaseolus vulgaris nodules in Tunisian fields

Fernández-Aunión, Cristina; Hamouda, Thouraya Ben; Iglesias‐Guerra, Fernando; Argandoña, Montserrat; Reina-Bueno, Mercedes; Nieto, Joaquı́n J.; Aouani, Mohamed Elarbi; Vargas, Carmen Regla

doi:10.1186/1471-2180-10-192

Cited by 46 publications

(37 citation statements)

References 58 publications

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“…In addition, it can accumulate mannitol if present in the external medium. The same compatible solute profile was recently reported for the strain R. etli 12a3, isolated from P. vulgaris nodules in Tunisian fields [6]. …”

Section: Discussionsupporting

confidence: 80%

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Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli

et al. 2012

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BackgroundThe compatible solute trehalose is involved in the osmostress response of Rhizobium etli, the microsymbiont of Phaseolus vulgaris. In this work, we reconstructed trehalose metabolism in R. etli, and investigated its role in cellular adaptation and survival to heat and desiccation stress under free living conditions.ResultsBesides trehalose as major compatible solute, R. etli CE3 also accumulated glutamate and, if present in the medium, mannitol. Putative genes for trehalose synthesis (otsAB/treS/treZY), uptake (aglEFGK/thuEFGK) and degradation (thuAB/treC) were scattered among the chromosome and plasmids p42a, p42c, p42e, and p42f, and in some instances found redundant. Two copies of the otsA gene, encoding trehalose-6-P-synthase, were located in the chromosome (otsAch) and plasmid p42a (otsAa), and the latter seemed to be acquired by horizontal transfer. High temperature alone did not influence growth of R. etli, but a combination of high temperature and osmotic stress was more deleterious for growth than osmotic stress alone. Although high temperature induced some trehalose synthesis by R. etli, trehalose biosynthesis was mainly triggered by osmotic stress. However, an otsAch mutant, unable to synthesize trehalose in minimal medium, showed impaired growth at high temperature, suggesting that trehalose plays a role in thermoprotection of R. etli. Desiccation tolerance by R. etli wild type cells was dependent of high trehalose production by osmotic pre-conditioned cells. Cells of the mutant strain otsAch showed ca. 3-fold lower survival levels than the wild type strain after drying, and a null viability after 4 days storage.ConclusionsOur findings suggest a beneficial effect of osmotic stress in R. etli tolerance to desiccation, and an important role of trehalose on the response of R. etli to high temperature and desiccation stress.

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Section: Discussionsupporting

confidence: 80%

“…The chemical shifts are reported in ppm on the δ scale relative to tetramethylsilane. Signals were assigned by comparison with previously published chemical shift values [6] and compared with 13 C-NMR of pure compounds.…”

Section: Methodsmentioning

confidence: 99%

Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli

et al. 2012

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“…The trehalose content of P. stutzeri 1501 cells grown in MM63 with either 50 mM or 700 mM NaCl was assayed enzymatically as described by FernandezAunión et al (16), using a method that involves the hydrolysis of trehalose by trehalase to two glucose molecules and the subsequent quantification of glucose by a coupled assay of glucose oxidase-peroxidase in the presence of o-toluidine. The oxidation of o-toluidine was monitored spectrophotometrically at 420 nm.…”

Section: Methodsmentioning

confidence: 99%

A Specialized Aspartokinase Enhances the Biosynthesis of the Osmoprotectants Ectoine and Hydroxyectoine in Pseudomonas stutzeriA1501

et al. 2011

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The compatible solutes ectoine and hydroxyectoine are widely produced by bacteria as protectants against osmotic and temperature stress. L-Aspartate-beta-semialdehyde is used as the precursor molecule for ectoine/ hydroxyectoine biosynthesis that is catalyzed by the EctABCD enzymes. L-Aspartate-beta-semialdehyde is a central intermediate in different biosynthetic pathways and is produced from L-aspartate by aspartokinase (Ask) and aspartate-semialdehyde-dehydrogenase (Asd). Ask activity is typically stringently regulated by allosteric control to avoid gratuitous synthesis of aspartylphosphate. Many organisms have evolved multiple forms of aspartokinase, and feedback regulation of these specialized Ask enzymes is often adapted to the cognate biochemical pathways. The ectoine/hydroxyectoine biosynthetic genes (ectABCD) are followed in a considerable number of microorganisms by an ask gene (ask_ect), suggesting that Ask_Ect is a specialized enzyme for this osmoadaptive biosynthetic pathway. However, none of these Ask_Ect enzymes have been functionally characterized. Pseudomonas stutzeri A1501 synthesizes both ectoine and hydroxyectoine in response to increased salinity, and it possesses two Ask enzymes: Ask_Lys and Ask_Ect. We purified both Ask enzymes and found significant differences with regard to their allosteric control: Ask_LysC was inhibited by threonine and in a concerted fashion by threonine and lysine, whereas Ask_Ect showed inhibition only by threonine. The ectABCD_ask genes from P. stutzeri A1501 were cloned and functionally expressed in Escherichia coli, and this led to osmostress protection. An E. coli strain carrying the plasmid-based ectABCD_ask gene cluster produced significantly more ectoine/hydroxyectoine than a strain expressing the ectABCD gene cluster alone. This finding suggests a specialized role for Ask_Ect in ectoine/hydroxyectoine biosynthesis.The growth arrest of microbial cells observed under severe high-osmolarity conditions is correlated with the reduction in the amount of free cytoplasmic water (12) and the reduction or collapse of turgor (7, 65). To promote water reentry and retention under high-osmolarity growth conditions and to balance turgor, many microorganisms amass a selected class of organic osmolytes, the compatible solutes (31, 66). Microbial cells accumulate compatible solutes through either synthesis or uptake from environmental resources (7, 65, 69). They can employ them not only as effective osmostress protectants, but also as protectants against heat (8, 10, 13, 17, 26) and cold (2, 25, 33) stress.The tetrahydropyrimidines ectoine and 5-hydroxyectoine ( Fig. 1) are an important class of compatible solutes (9,45,50). Biosynthesis of ectoine is catalyzed by L-2,4-diaminobutyric acid transaminase (EctB), N-␥-acetyltransferase (EctA), and ectoine synthase (EctC) (40,44). A subset of the ectoine producers hydroxylate ectoine to 5-hydroxyectoine (9, 17, 48) in a stereospecific fashion using the ectoine hydroxylase EctD (8, 9, 50). The structural genes (ectABC) for the ectoi...

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“…Although many of these cells are likely to have been dormant, many organisms can endure the effects of a water-limited environment by employing specific adaptation mechanisms that include (i) the accumulation of compatible solutes (e.g., trehalose, sucrose) and/or (ii) the production of exopolysaccharides. This has been demonstrated for key edaphic bacterial phyla, such as Proteobacteria43, Actinobacteria44 and Cyanobacteria23. In coastal deserts, such as the Namib and Atacama Deserts, moisture inputs such as fog and dew precipitation are fundamental in sustaining hot desert insect and plant populations4546, as well as microbial communities4748495051.…”

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confidence: 98%

Diel-scale temporal dynamics recorded for bacterial groups in Namib Desert soil

Gunnigle

Frossard

Ramond

et al. 2017

Sci Rep

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Microbes in hot desert soil partake in core ecosystem processes e.g., biogeochemical cycling of carbon. Nevertheless, there is still a fundamental lack of insights regarding short-term (i.e., over a 24-hour [diel] cycle) microbial responses to highly fluctuating microenvironmental parameters like temperature and humidity. To address this, we employed T-RFLP fingerprinting and 454 pyrosequencing of 16S rRNA-derived cDNA to characterize potentially active bacteria in Namib Desert soil over multiple diel cycles. Strikingly, we found that significant shifts in active bacterial groups could occur over a single 24-hour period. For instance, members of the predominant Actinobacteria phyla exhibited a significant reduction in relative activity from morning to night, whereas many Proteobacterial groups displayed an opposite trend. Contrary to our leading hypothesis, environmental parameters could only account for 10.5% of the recorded total variation. Potential biotic associations shown through co-occurrence networks indicated that non-random inter- and intra-phyla associations were ‘time-of-day-dependent’ which may constitute a key feature of this system. Notably, many cyanobacterial groups were positioned outside and/or between highly interconnected bacterial associations (modules); possibly acting as inter-module ‘hubs’ orchestrating interactions between important functional consortia. Overall, these results provide empirical evidence that bacterial communities in hot desert soils exhibit complex and diel-dependent inter-community associations.

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Biosynthesis of compatible solutes in rhizobial strains isolated from Phaseolus vulgaris nodules in Tunisian fields

Cited by 46 publications

References 58 publications

Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli

Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli

A Specialized Aspartokinase Enhances the Biosynthesis of the Osmoprotectants Ectoine and Hydroxyectoine in Pseudomonas stutzeriA1501

Diel-scale temporal dynamics recorded for bacterial groups in Namib Desert soil

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