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Abstract
Mercury (Hg) is extremely toxic for all living organisms. Hg-tolerant symbiotic rhizobia have the potential to increase legume tolerance, and to our knowledge, the mechanisms underlying Hg tolerance in rhizobia have not been investigated to date. Rhizobial strains of Ensifer medicae, Rhizobium leguminosarum bv. trifolii and Bradyrhizobium canariense previously isolated from severely Hg-contaminated soils showed different levels of Hg tolerance. The ability of the strains to reduce mercury Hg2+ to Hg0, a volatile and less toxic form of mercury, was assessed using a Hg volatilization assay. In general, tolerant strains displayed high mercuric reductase activity, which appeared to be inducible in some strains when grown at a sub-lethal HgCl2 concentration. A strong correlation between Hg tolerance and mercuric reductase activity was observed for E. medicae strains, whereas this was not the case for the B. canariense strains, suggesting that additional Hg tolerance mechanisms could be playing a role in B. canariense. Transcript abundance from merA, the gene that encodes mercuric reductase, was quantified in tolerant and sensitive E. medicae and R. leguminosarum strains. Tolerant strains presented higher merA expression than sensitive ones, and an increase in transcript abundance was observed for some strains when bacteria were grown in the presence of a sub-lethal HgCl2 concentration. These results suggest a regulation of mercuric reductase in rhizobia. Expression of merA genes and mercuric reductase activity were confirmed in Medicago truncatula nodules formed by a sensitive or a tolerant E. medicae strain. Transcript accumulation in nodules formed by the tolerant strain increased when Hg stress was applied, while a significant decrease in expression occurred upon stress application in nodules formed by the Hg-sensitive strain. The effect of Hg stress on nitrogen fixation was evaluated, and in our experimental conditions, nitrogenase activity was not affected in nodules formed by the tolerant strain, while a significant decrease in activity was observed in nodules elicited by the Hg-sensitive bacteria. Our results suggest that the combination of tolerant legumes with tolerant rhizobia constitutes a potentially powerful tool in the bioremediation of Hg-contaminated soils.
Highlights
Mercury is the most toxic heavy metal, and mercury contamination is becoming a major problem worldwide, in both wild ecosystems and agricultural soils
The minimum inhibitory concentration (MIC) values obtained for B. canariense in solid medium were higher than those previously reported, which had been measured in liquid medium (RuizDíez et al, 2012, 2013)
We analyzed the tolerance to Hg of several rhizobial strains collected from Hg-contaminated soils, and evaluated the role of mercuric reductase activity in the mercury tolerance of free-living bacteria and in the maintenance of nitrogen fixation in legume nodules subjected to mercury stress
Summary
Mercury is the most toxic heavy metal, and mercury contamination is becoming a major problem worldwide, in both wild ecosystems and agricultural soils. Mercury appears to enter in both prokaryotic and eukaryotic cells through ion channels, competing with essential metals such as copper, iron, or zinc (Blazka and Shaikh, 1992; Bridges and Zalups, 2005). It has a high affinity for the sulfhydryl groups of amino acids, causing the alteration and loss of function of enzymes and sulfur-containing antioxidants (Patra and Sharma, 2000; Nies, 2003). High bioaccumulation of mercury presents considerable problems in plants and animals, and results in prominent biomagnification in the trophic chain (David et al, 2012; Lavoie et al, 2013)
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