Coupled biogeochemical cycling of iron and manganese as mediated by microbial siderophores

Siderophores, biogenic chelating agents that facilitate Fe(III) uptake through the formation of strong complexes, also form strong complexes with Mn(III) and exhibit high reactivity with Mn (hydr)oxides, suggesting a pathway by which Mn may disrupt Fe uptake. In this review, we evaluate the major biogeochemical mechanisms by which Fe and Mn may interact through reactions with microbial siderophores: competition for a limited pool of siderophores, sorption of siderophores and metal–siderophore complexes to mineral surfaces, and competitive metal-siderophore complex formation through parallel mineral dissolution pathways. This rich interweaving of chemical processes gives rise to an intricate tapestry of interactions, particularly in respect to the biogeochemical cycling of Fe and Mn in marine ecosystems.     

Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp.

Seven strains of budding, non-prosthecate bacteria belonging to the Planctomyces/Pasteuria group and a Prosthecomicrobium sp. were examined for muramic and diaminopimelic acids. These typical components of Gram-negative murein were found only in Prosthecomicrobium strain IFAM 1314, but they could not be detected in seven budding bacteria. Electron micrographs of ultrathin cell wall sections of strains IFAM 1313 and 1317 showed a membrane with bilayer structure outside the cytoplasmic membrane. 10% sodium dodecylsulfate treatment (30 min, 100°C) allowed the isolation of highly stable cell sacculi which, upon chemical analysis, proved to be mainly proteinaceous. The budding bacteria also showed considerable resistance against penicillin G, ampicillin, cephalotin and D-cycloserin. Our data indicate that these bacteria lack an ordinary Gram-negative type of murein and, instead, carry a stable protein envelope.     

Transformation of iron and manganese in rice soils under different moisture regimes and organic matter applications

Summary Transformation of iron and manganese under three different moisture regimes,viz continuous waterlogged (W₁), continuous saturated (W₂) and alternate waterlogged and saturated (W₃) and three levels of organic matterviz 0, 0.5 and 1.0% in all possible combinations was studied in four soils. The results showed that under waterlogged moisture regime there was a sharp increase in the content of water soluble plus exchangeable manganese accompanied by significant decrease in the content of reducible manganese in all the soils excepting the acidic soil which was very poor in active manganese content. The increase in respect of iron in similar form was, however, very small. The increase in the content of water soluble plus exchangeable manganese as well as iron under the continuous saturated and alternate waterlogged and saturated moisture regimes was always much lower as compared to that under the continuous waterlogged condition. Application of organic matter brought about an increase in the content of water soluble plus exchangeable manganese in all the soils excepting the lateritic one irrespective of moisture regimes but did not cause any change in the content of iron and manganese in insoluble complex. The content of water soluble plus exchangeable iron and of insoluble ferrous iron although recorded some increase due to organic matter application, the increase was not so marked in any of the soils.     

The concentration of manganese,iron, and strontium in hip joint bone obtained from patients undergoing hip replacement surgery

The aim of this study was to determine the concentrations of manganese (Mn), iron (Fe) and strontium (Sr) in the cartilage with adjacent compact bone and spongy bone collected from patients after total hip replacement surgery. In addition, we examined relations between the concentrations of the metals in the bone and selected environmental factors. The concentration of Fe was the highest while Mn concentration was the lowest. The concentrations of Fe in the spongy bone in patients from larger cities were higher than in those living in smaller towns and villages. Significant correlations were found between Fe and Mn concentrations in the cartilage with adjacent compact bone and in the spongy bone, and between Mn and Sr in the spongy bone. In general, Mn, Fe and Sr concentrations in the bones of patients from NW Poland were lower than in other Polish regions and Europe, especially in industrialized countries. In conclusion, it seems that in addition to routine monitoring of the abiotic environment, it is essential to monitor concentrations of heavy metals having a long-term impact in humans.     

Battles with iron: manganese in oxidative stress protection

The redox-active metal manganese plays a key role in cellular adaptation to oxidative stress. As a cofactor for manganese superoxide dismutase or through formation of non-proteinaceous manganese antioxidants, this metal can combat oxidative damage without deleterious side effects of Fenton chemistry. In either case, the antioxidant properties of manganese are vulnerable to iron. Cellular pools of iron can outcompete manganese for binding to manganese superoxide dismutase, and through Fenton chemistry, iron may counteract the benefits of non-proteinaceous manganese antioxidants. In this minireview, we highlight ways in which cells maximize the efficacy of manganese as an antioxidant in the midst of pro-oxidant iron.     

Effect of algal growth on the availability of phosphorus,iron and manganese in rice soils

Summary Laboratory experiments were conducted to study the effect of algal growth on the change of (I) pH, (II) available phosphorus and (III) solubility of iron and manganese content in five waterlogged alluvial rice soils of West Bengal, India. The results showed that the algal growth initially caused an increase in the soil pH, which later declined to the original value in some of the soils. The available phosphorus content decreased upto 90 days of their growth and began to increase towards the later period of incubation. The drastic fall of water soluble plus exchaneable manganese content of the soils due to algal growth was accompanied by similar increase in reducible manganese content. No appreciable change in water soluble plus exchangeable ferrous iron content was encountered but theN-NH₄OAC(pH 3) extractable iron due to algal growth progressively decreased with the progress of the incubation period.     

Effects of iron deficiency and iron overload on manganese uptake and deposition in the brain and other organs of the rat

Managanese (Mn) is an essential trace element at low concentrations, but at higher concentrations is neurotoxic. It has several chemical and biochemical properties similar to iron (Fe), and there is evidence of metabolic interaction between the two metals, particularly at the level of absorption from the intestine. The aim of this investigation was to determine whether Mn and Fe interact during the processes involved in uptake from the plasma by the brain and other organs of the rat. Dams were fed control (70 mg Fe/kg), Fe-deficient (5–10 mg Fe/kg), or Fe-loaded (20 g carbonyl Fe/kg) diets, with or without Mn-loaded drinking water (2 g Mn/L), from day 18–19 of pregnancy, and, after weaning the young rats, were continued on the same dietary regimens. Measurements of brain, liver, and kidney Mn and nonheme Fe levels, and the uptake of⁵⁴Mn and⁵⁹Fe from the plasma by these organs and the femurs, were made when the rats were aged 15 and 63 d. Organ nonheme Fe levels were much higher than Mn levels, and in the liver and kidney increased much more with Fe loading than did Mn levels with Mn loading. However, in the brain the increases were greater for Mn. Both Fe depletion and loading led to increased brain Mn concentrations in the 15-d/rats, while Fe loading also had this effect at 63 d. Mn loading did not have significant effects on the nonheme Fe concentrations.⁵⁴Mn, injected as MnCl₂ mixed with serum, was cleared more rapidly from the circulation than was⁵⁹Fe, injected in the form of diferric transferrin. In the 15-d-rats, the uptake of⁵⁴Mn by brain, liver, kidneys, and femurs was increased by Fe loading, but this was not seen in the 63-d rats. Mn supplementation led to increased⁵⁹Fe uptake by the brain, liver, and kidneys of the rats fed the control and Fe-deficient diets, but not in the Fe-loaded rats. It is concluded that Mn and Fe interact during transfer from the plasma to the brain and other organs and that this interaction is synergistic rather than competitive in nature. Hence, excessive intake of Fe plus Mn may accentuate the risk of tissue damage caused by one metal alone, particularly in the brain.     

Iron and manganese complexes of benzothiazolyformazans

A series of Iron (Fe(II)) and manganese (Mn(II)) complexes of 1,3-substituted 5-(2-benzothiazolyl)formazans are reported. The crystal structures of the Fe(II) and Mn(II) complexes of 1,3-diphenyl-5-(2-benzothiazolyl)formazan are very similar and both contain a coordination sphere of four five-membered rings involving the N¹ and N³ nitrogen atoms of the formazan chain and the N² of the heterocyle resulting in a distorted octahedral structure in both cases. The distortions arise primarily from the spatial requirements of the bulky phenyl substituents.     

Effect of calcium carbonate and organic matter on the growth and concentration of iron and manganese in sorghum (Sorghum bicolor)

Summary The effect of CaCO₃ and organic matter on the availability of iron and manganese was studied on sorghum (Sorghum bicolor). Addition of calcium carbonate caused significant decrease in dry matter and grain yield. But yields tended to increase with the addition of organic matter at the rate of 15 t/ha. The iron concentration decreased with the addition of CaCO₃ at all the stages of crop growth. Like iron, concentration of manganese also decreased with the increase in added CaCO₃. Organic matter increased the iron concentration both at seedling and flowering stage. The concentration of manganese was, however, dependent on the stage of the crop.     

Differential response of salt-marsh species to variation of iron and manganese

Salt-marsh plants of the lower, middle and upper marsh were compared in their response to iron and manganese. The species studied showed differential sensitivity to high concentrations of Fe (1 000 μM) and Mn (10 000 μM) in hydroculture experiments, species of the lower marsh being more resistant than species of the upper marsh. Fe and Mn concentrations in the root were higher than in the shoot, which was also found in plants inundated with seawater. High Fe and Mn concentrations in the root are probably the result of the oxidizing power of plant roots with a subsequent low translocation of Fe (II) and Mn (II) to the shoot. At high (toxic) Fe and Mn levels in the nutrient solution, Fe and Mn concentrations were much higher in the shoots of sensitive species than in resistant species. The P content of roots and shoots was not influenced by increased Fe and Mn concentrations. Fe and Mn resistance in Spartina anglica and Juncus gerardii, may be in part due to a high root porosity. Other species, however, that are similarly resistant to Fe and Mn lack a well-developed aerenchym. Root porosity, radial oxygen loss and Fe (II) and Mn (II) exclusion by oxidation to Fe (III) (hydr)oxides deposited on the roots form part of the resistance mechanism of hygrohalophytes to Fe and Mn; the differences in this respect between the species may also be due to other metabolic aspects.     

Transformations in plant-available forms of iron and manganese as influenced by manuring and cropping under irrigation

Summary Vertisols from field plots fertilized continuously with P, K, FYM alone and in combination at the rate of 60 kg P₂O₅, 30 kg K₂O and 1.5 ton FYM per ha were tested for different forms of Fe and Mn as a consequence of continuous cropping with sorghum and wheat. The transformations that occurred in different forms of plant-available iron were greater than those of Mn. Exchangeable and easily reducible Fe contents were markedly influenced by treatments. In manganese, transformations of easily reducible to exchangeable forms were conspicuous.     

Characterization of extracellular polymers synthesized by tropical intertidal biofilm bacteria

AIM: This study was performed to determine the potential of tropical intertidal biofilm bacteria as a source of novel exopolymers (EPS). METHODS AND RESULTS: A screening procedure was implemented to detect EPS-producing biofilm bacteria. Isolates MC3B-10 and MC6B-22, identified respectively as a Microbacterium species and Bacillus species by 16S rDNA and cellular fatty acids analyses, produced different EPS, as evidenced by colorimetric and gas chromatographic analyses. The polymer produced by isolate MC3B-10 displays significant surfactant activity, and may chelate calcium as evidenced by spectroscopic analysis. CONCLUSIONS: Polymer MC3B-10 appears to be a glycoprotein, while EPS MC6B-22 seems to be a true polysaccharide dominated by neutral sugars but with significant concentrations of uronic acids and hexosamines. EPS MC3B-10 possesses a higher surfactant activity than that of commercial surfactants, and given its anionic nature, may chelate cations thus proving useful in bioremediation. The chemical composition of polymer MC6B-22 suggests its potential biomedical application in tissue regeneration. SIGNIFICANCE AND IMPACT OF THE STUDY: This is the first report of a Microbacterium species producing EPS with surfactant properties, which expands our knowledge of the micro-organisms capable of producing these biomolecules. Furthermore, this work shows that tropical intertidal environments are a nonpreviously recognized habitat for bioprospecting EPS-producing bacteria, and that these molecules might be involved in ecological roles protecting the cells against dessication.     

The neurotoxicity of iron,copper and manganese in Parkinson's and Wilson's diseases

Impaired cellular homeostasis of metals, particularly of Cu, Fe and Mn may trigger neurodegeneration through various mechanisms, notably induction of oxidative stress, promotion of α-synuclein aggregation and fibril formation, activation of microglial cells leading to inflammation and impaired production of metalloproteins. In this article we review available studies concerning Fe, Cu and Mn in Parkinson's disease and Wilson's disease. In Parkinson's disease local dysregulation of iron metabolism in the substantia nigra (SN) seems to be related to neurodegeneration with an increase in SN iron concentration, accompanied by decreased SN Cu and ceruloplasmin concentrations and increased free Cu concentrations and decreased ferroxidase activity in the cerebrospinal fluid. Available data in Wilson's disease suggest that substantial increases in CNS Cu concentrations persist for a long time during chelating treatment and that local accumulation of Fe in certain brain nuclei may occur during the course of the disease. Consequences for chelating treatment strategies are discussed.     

Two proton-one electron coupled transfer in iron and manganese superoxide dismutases: A density functional study

A theoretical study on a simple model has been carried out to contribute to the elucidation of the reaction mechanism of iron and manganese superoxide dismutases (FeSOD and MnSOD). The presence of the water molecule in the reaction is very important since it is involved in a transfer process. In fact, this step is a complex coupled transfer process that involves two protons and one electron at the same time. This step is possible in a specific arrangement of superoxide anion in its coordination to the transition metal ion. The other possible conformations are the inactive species that evolves to the active complex in a slow way or that accepts an additional proton to produce a new species (“dead-end” complex) that is unable to evolve to hydrogen peroxide. Time-dependent formalism applied to the density functional calculations and compared to the experimental electronic spectra has allowed us to choose some possible candidates for the “dead-end” complex. Our results indicate that a hydroperoxo form (4-Mn) is the more probable candidate to it. However, other possibilities cannot be rejected.     

Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls

Six morphotypes of small mussels (Bivalvia: Mytilidae) were found attached to naturally sunken wood collected in the Bohol Sea (Philippines). These specimens are related to the large Bathymodiolus mussels that are found worldwide at cold seeps and hydrothermal vents. In these habitats, the mytilids harbour sulphur- and methane-oxidizing endosymbionts in their gills and depend on the energy and carbon provided by the symbionts. In this study, bacteria associated with the gills of wood-associated mussels are characterized using molecular and microscopic techniques. The existence of bacteria in the lateral zone of gill filaments in all specimens is demonstrated. Comparative analyses of 16S rRNA gene and adenosine 5'-phosphosulphate (APS) reductase gene sequences indicate that the bacteria are closely related to sulphur-oxidizing endosymbionts of Bathymodiolus. FISHs using specific probes confirm that sulphur oxidizers are by far the most abundant, if not the only bacteria present. Electron micrographs displayed mostly extracellular bacteria located between microvilli at the apical surface of host gill epithelial cells all along the lateral zone of each gill filament. In some specimens, occasional occurrence of intracellular bacteria with similar morphology was noted. This study provides the first molecular evidence for the presence of possible thiotrophic symbiosis in sunken wood ecosystems. With their epibiotic bacteria, wood-associated mussels display a less integrated type of interaction than described in their seep, vent and whale fall relatives.     

Boron,copper, iron,manganese and zinc contents in leaves of flowering sunflower plants (Helianthus annuus,L.), grown with different boron supplies

Summary Boron, copper, iron, manganese and zinc concentrations were measured in sunflower leaves from plants grown hydroponically in a closed continuous flow system and with boron concentrations ranging from deficient to toxic. Leaves were analyzed at the stage of flower development. There was a highly significant inverse correlation between B concentration in solution and Mn concentration in leaves. Cu, Fe and Zn concentrations in the leaves were not changed by the different B levels, although the B concentration in leaves increased with an increasing concentration in solution, showing a close correlation each other.     

Role of menaquinone in the reduction of fumarate, nitrate, iron(III) and manganese(IV) by Shewanella putrefaciens MR-1

Abstract Mutants of Shewanella putrefaciens MR-1 deficient in menaquinone and methylmenaquinone, but which have wild-type levels of ubiquinone, retain the ability to use trimethylamine N -oxide as an electron acceptor, but they lose the ability to use nitrate, iron(III), and fumarate as electron acceptors. These mutants also show a reduced rate of manganese(IV) reduction. One of these mutants could be restored to essentially wild-type phenotype by supplementing the medium with 1,4-dihydroxy-2-naphthoic acid. A requirement for naphthoquinones in iron(III) reduction and a preference for naphthoquinones in manganese(IV) reduction provide further support that the metal reducing systems in MR-1 are linked to anaerobic respiration.     

Surface iron polymers and hydroxy acids. A model of iron supply in sideramine-free fungi

Biochemical and electron microscopic evidence is presented that sideramine-free fungi form iron hydroxide polymer layers on the cell surface when grown in an iron containing medium.Iron hydroxide polymer formation on the cell surface is completely prevented in sideramine producing strains of Neurospora crassa. After feeding a sideramine-free mutant of Neurospora crassa with ornithine in order to restore the sideramine synthesis the iron hydroxide coat is gradually dissolved.The addition of excess citrate and malate to the incubation medium also prevents iron polymer adsorption, suggesting that hydroxy acids may be involved in iron supply, when sideramine-free organisms are grown in iron containing media.In order to study the interaction between iron hydroxide polymer deposition upon the cell surface and iron chelating acids in Neurospora crassa, the amount and the proportion of excreted acids was studied under various experimental conditions. Gas chromatographic analysis of the acids produced under iron deficient conditions revealed that succinate, malate and citrate were present within the cells in the early growth phase. The acids were sequentially excreted into the medium in the order succinate, malate and citrate. The amount of succinate decreased after 2 days of cultivation, whereas the amount of malate and citrate continually increased. Although citrate was present within the cells from the 1st day, excretion occurred very late, generally after the 3rd day.It is suggested that sideramine-free fungi first adsorb iron as a hydroxide polymer on the cell surface, and that it is gradually solubilized by excreted hydroxy acids such as citrate or malate. Thus high local concentrations of iron chelated by hydroxy acids provide sideramine-free fungi with a continuous iron supply.Abbreviations BSTFA N,O-Bis(trimethylsilyl)-trifluoracetamide - GC Gaschromatography - EGTA Ethylenglykol-bis(2-aminoethylether) N,N-tetraacetic acid - TMS Trimethylsilyl