Attenuation of metal toxicity by frankial siderophores
27 Jul 2010-Toxicological & Environmental Chemistry (Taylor & Francis Group)-Vol. 92, Iss: 7, pp 1339-1346
TL;DR: Siderophores minimize the metal-induced inhibition of growth in Frankia, likely due to regulation of nutritional imbalances and metabolic processes during adaptation towards metal stress and/or metal toxicity.
Abstract: In order to investigate the role of frankial siderophores in minimizing metal toxicity, Frankia strains were grown at different concentrations of Mg2+, Cu2+, and Zn2+. Growth was observed up to 500 µmol L−1 Mg2+, 10 µmol L−1 Cu2+, and 10 µmol L−1 Zn2+ while the maxima were at 200 µmol L−1 Mg2+, 1 µmol L−1 Cu2+, and 1 µmol L−1 Zn2+. The siderophore production was increased up to 500 µmol L−1 Mg2+, 10 µmol L−1 Cu2+, 100 µmol L−1 (hydroxamate type), and 200 µmol L−1 (catecholate type) Zn2+ while maximum production was found at Mg2+ (200 µmol L−1), Cu2+ (10 µmol L−1), and Zn2+ (10 µmol L−1). The results suggested that the growth was protected at higher concentrations of Mg2+ (up to 500 µmol L−1), Cu2+ (10 µmol L−1), and Zn2+ (10 µmol L−1), possibly due to enhanced siderophore production. Thus, siderophores minimize the metal-induced inhibition of growth in Frankia, likely due to regulation of nutritional imbalances and metabolic processes during adaptation towards metal stress and/or metal toxicity.
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TL;DR: Each strain had a unique combination of metal import, binding, modification, and export genes that explain differences in patterns of metal resistance between strains.
Abstract: Frankia are actinobacteria that form a symbiotic nitrogen-fixing association with actinorhizal plants, and play a significant role in actinorhizal plant colonization of metal contaminated areas. Many Frankia strains are known to be resistant to several toxic metals and metalloids including Pb2+, Al+3, SeO2, Cu2+, AsO4, and Zn2+. With the availability of eight Frankia genome databases, comparative genomics approaches employing phylogeny, amino acid composition analysis, and synteny were used to identify metal homeostasis mechanisms in eight Frankia strains. Characterized genes from the literature and a meta-analysis of 18 heavy metal gene microarray studies were used for comparison. Unlike most bacteria, Frankia utilize all of the essential trace elements (Ni, Co, Cu, Se, Mo, B, Zn, Fe, and Mn) and have a comparatively high percentage of metalloproteins, particularly in the more metal resistant strains. Cation diffusion facilitators, being one of the few known metal resistance mechanisms found in the Frankia genomes, were strong candidates for general divalent metal resistance in all of the Frankia strains. Gene duplication and amino acid substitutions that enhanced the metal affinity of CopA and CopCD proteins may be responsible for the copper resistance found in some Frankia strains. CopA and a new potential metal transporter, DUF347, may be involved in the particularly high lead tolerance in Frankia. Selenite resistance involved an alternate sulfur importer (CysPUWA) that prevents sulfur starvation, and reductases to produce elemental selenium. The pattern of arsenate, but not arsenite, resistance was achieved by Frankia using the novel arsenite exporter (AqpS) previously identified in the nitrogen-fixing plant symbiont Sinorhizobium meliloti. Based on the presence of multiple tellurite resistance factors, a new metal resistance (tellurite) was identified and confirmed in Frankia. Each strain had a unique combination of metal import, binding, modification, and export genes that explain differences in patterns of metal resistance between strains. Frankia has achieved similar levels of metal and metalloid resistance as bacteria from highly metal-contaminated sites. From a bioremediation standpoint, it is important to understand mechanisms that allow the endosymbiont to survive and infect actinorhizal plants in metal contaminated soils.
25 citations
Cites background from "Attenuation of metal toxicity by fr..."
...The effects of metals on Frankia physiology have been investigated in culture [10,11], in planta [12,13], and in the field [14-16]....
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TL;DR: The results suggest that the siderophore produced by Anabaena oryzae can act as a biological sequestering agent for the mitigation of cadmium metal ions from the paddy fields to improve crop productivity.
Abstract: The efficacy of dihydroxamate siderophore in attenuation/mitigation of cadmium toxicity, an optimum level of cadmium under which cyanobacterium can grow and produce siderophore, complexation behaviour of cadmium and siderophore and kinetics of complexation along with in silico analysis have been investigated in paddy field cyanobacterium Anabaena oryzae under iron replete and deplete conditions. Results showed that cadmium concentration as 1.0 μM is optimum for growth as well as siderophore production in iron replete and deplete culture conditions. The complexation between cadmium–siderophore was evident in spectral scan. Kinetic studies as well as in silico docking analysis indicate that like iron, cadmium also forms a thermodynamically stable complex with siderophore. Thus our results suggest that the siderophore produced by Anabaena oryzae can act as a biological sequestering agent for the mitigation of cadmium metal ions from the paddy fields to improve crop productivity.
23 citations
TL;DR: The present study provides the first comprehensive overview of the complexity of Frankia's ligandosphere and opens a path to a deeper understanding of mechanisms that regulate metal homeostasis in frankiae.
Abstract: Frankia spp. are widespread nitrogen-fixing soil bacteria, which often live in symbiosis with a broad range of hosts. Metal homeostasis plays a crucial role in the success of the symbiosis regarding the acquisition of essential trace metals and detoxification of potentially toxic elements. We have hypothesised that Frankia releases many organic ligands with a broad spectrum of affinity for essential and toxic metals. We coined the term ‘ligandosphere’ to describe the entirety of excreted metal complexing agents and ligands derived from the dissolved organic matter. Using metal isotope-coded profiling (MICP); metallophores of physiological important and toxic trace metals were identified by the addition of stable metal isotope pairs such as 54Fe/58Fe, 63Cu/65Cu, 66Zn/68Zn or 95Mo/98Mo. Liquid chromatography coupled to a mass spectrometer revealed strong variations of the metallophore profile in between the 14 test-strains. In total, about 83 organic ligands were identified as binding to one of the tested metals. The predicted sum formula of the major Fe binding ligands and MS/MS experiments suggested that several metallophore candidates have a similar molecular backbone. Growth experiments with a hyper-producer of metallophores revealed a positive relationship between metallophore production and the concentration of Cu in the growth medium. The present study provides the first comprehensive overview of the complexity of Frankia's ligandosphere. It opens a path to a deeper understanding of mechanisms that regulate metal homeostasis in frankiae. Deciphering these mechanisms is important since the fitness of actinorhizal plants and their potential in ecological restoration relies heavily on their symbiosis with frankiae.
20 citations
TL;DR: The basic understanding of the functioning and properties of Fur protein along with its role, interaction and regulation at various levels in cyanobacteria has been discussed in detail.
Abstract: The Ferric uptake regulator (Fur) protein is a global iron regulator found in most prokaryotes. Although the Fur protein is involved in a variety of metabolic pathways, it is specifically known for the regulation of several iron responsive genes. It binds to the highly conserved sequences located in the upstream promoter region known as iron boxes, using ferrous ion as a co-repressor. Apart from that, the Fur protein is also directly/indirectly involved in a variety of other crucial physiological pathways. Hence, understanding the mechanism of action and the mechanistic pathways of iron regulation by Fur is necessary and important. The basic understanding of the functioning and properties of Fur protein along with its role, interaction and regulation at various levels in cyanobacteria has been discussed in detail.
15 citations
Cites background from "Attenuation of metal toxicity by fr..."
...Iron is considered to be one of the essential elements required for the growth and maintenance of cellular metabolism in a wide diversity of prokaryotes (Meyer 2000; Singh et al. 2008, 2010), the exception being members of the genus Lactobacillus (Archibald 1983)....
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TL;DR: Results suggest that the physiological approaches i.e., nitrogenase activity, glutamine synthetase activity and ammonia excretion are strain specific and might be helpful in rapid identification, in designing the marker for the specific strains as well as in improving nitrogen fixation in agroforestry.
Abstract: Different Frankia strains (HsIi2, HsIi4, HsIi5, HsIi8, HsIi9, HsIi10, HsIi11, HsIi12, HsIi13, HsIi14) nodulating Hippophae salicifolia D. Don, were characterized on the basis of physiological, biochemical and molecular attributes. Results suggest that the physiological approaches i.e., nitrogenase activity, glutamine synthetase (GS) activity and ammonia excretion are strain specific. The highest rate of nitrogen fixation and maximum production of ammonia with low GS makes the strain HsIi11, a suitable biofertilizer as compared to other strains. Analysis of total protein pattern (SDS–PAGE) revealed that the most closely related strains HsIi10 and HsIi4 were found to be most distantly related to the most similar strains HsIi14, HsIi5, HsIi13, HsIi11 and HsIi12. RAPD PCR analyses with an arbitrary primer 1253 produced distinct, unique and specific DNA fingerprints for each of the Frankia strain and 100% polymorphism was observed which uncovers the genetic diversity. These approaches might be helpful in rapid identification, in designing the marker for the specific strains as well as in improving nitrogen fixation in agroforestry.
13 citations
Cites background from "Attenuation of metal toxicity by fr..."
...... economic value not only in terms of restoration of soil fertility along the fragile mountain slopes thereby obstructing erosion and landslides but also serve as a major source for meeting the increasing demand for fuel wood and fodder requirements (Rongsen 1992; Tsai and Benson 1989; Kato et al. 2007), particularly of people dwelling along high-altitude regions of the Eastern Himalayas with limited natural resources (Sarma et al. 2006; Singh ......
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References
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Journal Article•
TL;DR: Procedures are described for measuring protein in solution or after precipitation with acids or other agents, and for the determination of as little as 0.2 gamma of protein.
289,852 citations
"Attenuation of metal toxicity by fr..." refers methods in this paper
...The growth was monitored in terms of protein content, determined as per the procedure of Lowry et al. (1951) using bovine serum albumin as standard....
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TL;DR: A broad overview of the evidence for an involvement of each mechanism in heavy metal detoxification and tolerance is provided.
Abstract: Heavy metals such as Cu and Zn are essential for normal plant growth, although elevated concentrations of both essential and non-essential metals can result in growth inhibition and toxicity symptoms. Plants possess a range of potential cellular mechanisms that may be involved in the detoxification of heavy metals and thus tolerance to metal stress. These include roles for the following: for mycorrhiza and for binding to cell wall and extracellular exudates; for reduced uptake or efflux pumping of metals at the plasma membrane; for chelation of metals in the cytosol by peptides such as phytochelatins; for the repair of stress-damaged proteins; and for the compartmentation of metals in the vacuole by tonoplast-located transporters. This review provides a broad overview of the evidence for an involvement of each mechanism in heavy metal detoxification and tolerance.
2,751 citations
"Attenuation of metal toxicity by fr..." refers background in this paper
...But the enhanced siderophore production would be capable of protecting the cells from metal toxicity, and growth was visualized at the reduced rate (more than the control) by maintaining the minimum concentration of the metals into the frankial cells through efflux and influx transporters or pumps (Hall, 2002; Jing, He, and Yang 2007)....
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...Similarly, several types of transporter proteins are synthesized at the higher concentrations of Zn2þ to maintain and regulate its intracellular levels in bacteria (Hall 2002; Jing, He, and Yang 2007)....
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...…would be capable of protecting the cells from metal toxicity, and growth was visualized at the reduced rate (more than the control) by maintaining the minimum concentration of the metals into the frankial cells through efflux and influx transporters or pumps (Hall, 2002; Jing, He, and Yang 2007)....
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...Excessive metal concentrations in soil and water cause impaired metabolism and reduction in the growth of plants (Hall 2002; Jing, He, and Yang 2007)....
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...They are also involved in electron transfer, signal transduction, and membrane stabilization, and act as components of various enzymes (Hall 2002; Romani and Maguire 2002)....
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TL;DR: The complement of efflux systems of 63 sequenced prokaryotes was compared with that of the heavy metal resistant bacterium Ralstonia metallidurans and showed that heavy metal resistance is the result of multiple layers of resistance systems with overlapping substrate specificities, but unique functions.
Abstract: What makes a heavy metal resistant bacterium heavy metal resistant? The mechanisms of action, physiological functions, and distribution of metal-exporting proteins are outlined, namely: CBA efflux pumps driven by proteins of the resistance–nodulation–cell division superfamily, P-type ATPases, cation diffusion facilitator and chromate proteins, NreB- and CnrT-like resistance factors. The complement of efflux systems of 63 sequenced prokaryotes was compared with that of the heavy metal resistant bacterium Ralstonia metallidurans. This comparison shows that heavy metal resistance is the result of multiple layers of resistance systems with overlapping substrate specificities, but unique functions. Some of these systems are widespread and serve in the basic defense of the cell against superfluous heavy metals, but some are highly specialized and occur only in a few bacteria. Possession of the latter systems makes a bacterium heavy metal resistant.
1,333 citations
"Attenuation of metal toxicity by fr..." refers background in this paper
...…(ABC) transporters, metal efflux pumps, and unspecific membrane transporters present in some bacteria which either efflux toxic or over concentrated metals, or maintain low intracellular metal ions (Nies 1995; Borges-Walmsley, McKeegean, and Walmsley 2003; Nies 2003; Haferburg and Kothe 2007)....
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...transporters present in some bacteria which either efflux toxic or over concentrated metals, or maintain low intracellular metal ions (Nies 1995; Borges-Walmsley, McKeegean, and Walmsley 2003; Nies 2003; Haferburg and Kothe 2007)....
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1,299 citations
"Attenuation of metal toxicity by fr..." refers methods in this paper
...Absorbance of the aliquots was measured at 526 nm and was referred to a standard curve prepared with hydroxylamine HCl. Catecholate type siderophore was determined in the above lypholized culture supernatant (mg catecholate per mg protein) according to Arnow (1937)....
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TL;DR: Soil salinity is one of the most significant abiotic stresses for plant agriculture and genetically improving the salt tolerance of crop plants is an important part of basic plant biology, contributing to the understanding of subjects.
Abstract: Soil salinity is one of the most significant abiotic stresses for plant agriculture. Apart from the practical goal of genetically improving the salt tolerance of crop plants, salt tolerance research represents an important part of basic plant biology, contributing to our understanding of subjects
712 citations