Evolutionary Role Of Iron

Journal of Evolutionary Biochemistry and Physiology, Vol. 37, No. 4, 2001, pp. 444—450. Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 37, No. 4, 2001, pp. 338—343. Original Russian Text Copyright © 2001 by Verkhovtseva, Filina, Pukhov.

PROBLEM PAPERS

Evolutionary Role of Iron in Metabolism of Prokaryotes and in Biogeochemical Processes1 Yu. V. Verkhovtseva*, Ya. Yu. Filina**, and D. E. Pukhov** * Lomonosov State University, Moscow, Russia ** Demidov State University, Yaroslavl, Russia Received April 12, 2000

Abstract—The paper reviews data summarizing points of view about the “conceptual” role of iron in the appearance and evolutionary formation of the Earth and its biosphere. Partici pation of iron and its compounds in the appearance and development of processes of anaero- and aerobiosis as fundamental “blocks” of metabolism is presented as a hierarchical scheme. Magnetically arrayed iron compounds, in which the element is both in the Fe(II) and in the Fe(III) state, are considered a connecting link between the hierarchical levels. It is shown that the energy transformation Fe(II) ↔ Fe(III) is an oxidation–reduction energy core of the most important metabolic iron complexes and of processes of biogenesis both at the cellular level and in biogeosystems.

IMPORTANCE OF IRON IN FORMATION OF BIOSPHERE ON THE EARTH According to modern concepts of some geologists, geochemists, biochemists, and microbiologists, the whole evolution of the Earth and possibility of origin of life on it depended essentially on the ratio of Fe and FeO in the Earth crust [1– 4], i.e., on the ratio of amounts of metallic iron and Fe(II), which in the primordial Earth matter amounted to 13 and 24%, respectively. In the early Earth history these iron forms were the main absorbents of oxygen formed at photolysis of water, the metallic iron amount decreasing in the process of its transformation into the Fe(II) state. In the arising anoxygenic prokaryotic life (about 4 bln years ago) the iron was used in the form of Fe(II) compounds (for example, FeSproteins and ferredoxin (EC 1.8.7.1)) as electron carriers in strict heterotrophic anaerobic fermentators [5].

The subsequent accumulation of oxygen in atmosphere (due to oxygenic photosynthesis by cyanobacteria) was accompanied by its binding by Fe(II) iron oxide and conversion to Fe(III). With the accumulation of free oxygen in the Earth atmosphere a shift to the next oxygenic stage of life evolution, iron was included in metabolic pathways both in the Fe(II), and in Fe(III) state. The importance of such compounds is due to ability of their “iron–oxide” core to accept or release electrons in the course of transformation Fe(II) ↔ Fe(III), which, thereby, is the energy center. Partici pation in diverse oxidation– reduction reactions determines the essential importance of iron complexes both at the level of metabolic transformations in the cell, and in biogeochemical processes. These levels are considered below in a greater detail. 1 The paper is published as a matter of discussion.

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EVOLUTIONARY ROLE OF IRON IN METABOLISM OF PROKARYOTES

BIOCHEMICAL PROCESSES OF IRON TRANSFORMATIONS AT THE CELLULAR LEVEL The iron occupies a special place among 12 macroelements necessary for the life activity of both prokaryotic, and eukaryotic organisms at a relatively high (> 10–4 M) concentration. The significant role of iron in metabolism is due to its peculiarity as a transient element that can easily change its oxidation degree, Fe(II) or Fe(III). It allows iron to coordinate various electron donors (coordination ligands) and to partici pate in various oxidation–reduction processes. Ligands form various surrounding of the core, which determines formation of iron complexes, particularly, of iron-containing proteins, in nature. Owing to the wide occurrence, as well as to their properties, these compounds were included in fundamental processes of metabolism in organisms: in DNA synthesis (ribonucleoside di phosphate reductase (EC 1.17.4.1) and ribonucleoside tri phosphate reductase (EC 1.17.4.2)), in photosynthesis, respiration, nitrogen fixation, and some others [6]. At present, more than 20 of such metabolically important biocomplexes have been known. As compared with other metals (Mg, Ca, Co, Cu, Zn, Mo) forming metallobiomolecules in organisms, only iron forms such diversity of biocomplexes [7]. In the scheme I we have tried to present the main stages of evolution of biosphere, anaerobic and aerobic, and to specify fundamental processes of life activity of prokaryotes and the protein iron complexes that determine the occurrence of these processes. Considering evolutionary development of prokaryotes, bacteria and cyanobacteria, that prevail on the Earth during more than 3 bln years and are “test objects of the Nature” in its search for optimal biochemical pathways of metabolism, a direct partici pation of iron compounds can be noted in this natural selection of metabolism. Indeed, protein complexes of iron partici pate in all fundamental processes of the life activity both at anaerobic, and at aerobic stages of evolution of biosphere (scheme I). Thus, such “ancient” protein complexes of iron, as FeS-proteins, ferredoxin, rubredoxin (EC

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1.18.1.1), hydrogenase (EC 1.18.99.1), cytochrome c oxidase (EC 1.9.3.1), are involved in the most important energy processes of anaerobiosis, fermentation evolutionary more recent photosynthesis in eubacteria. The same enzymes provide anaerobic nitrogen fixation. The iron-containing enzymes are also necessary in anaerobic respiration: “nitrate” and “sulfate”: nitrate reductase (EC 1.7.99.4) and nitrite reductase (EC 1.7.99.3), and hydrogenase, respectively. Besides, there are processes of biogenesis of iron compounds at the anaerobic stage of life, i.e., extra- and intracellular formation of iron minerals with partici pation of bacteria. More than 10 such biominerals have been described [8]. Of a special interest is the ferrimagnetic mineral magnetite (FeO2 • Fe2O3) that is composed both of Fe(II), and of Fe(III), i.e., at the biochemical level the gradient (microaerobic) conditions occur, under which the energy balance in relation to the iron mineral formation is determined by the ratio Fe(II) : Fe(III). The problem of the biomineralization process and the magnetite biogenesis is considered below in a greater detail. In the oxygen atmosphere, spectrum of iron complexes partici pating in metabolism of prokaryotes was extended, while Fe-enzymes of anaerobic stage of the biosphere development were preserved. By their example it is possible to follow “the evolution itself that looks like a gradual complication, whose previous stage is included in the subsequent one as a necessary constituent” [9]. Thus, the aerobic transport chain was composed of iron-containing dehydrogenases: succinate dehydrogenase (EC 1.2.1.16), NADH dehydrogenase (EC 1.6.99.2), formiate dehydrogenase (EC 1.2.1.43), and cytochromes. The defense from reaction oxygen compounds was required, so such iron complexes as superoxide dismutase (EC 1.15.1.1), xanthine oxidase (EC 1.2.3.2), catalase (EC 1.11.1.6), peroxidase (EC 1.11.1.7) were “selected” in the process of evolution to perform this task. Cofactor of the above-listed enzymes is iron with the (III) oxidation state, whose reversible reduction to Fe(II) determines their functioning. Besides, catalase and peroxidase contain iron in the heme structure. The oxygen stage of the nitrogen cycle, apart from Fe-enzymes partici pating in anaerobic ni-

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trogen fixation, includes leghemoglobin (EC 1.6.2.6), providing oxygen binding and defense of the nitrogenase complex of symbiotic nitrogen fixers from its reaction action. As a whole, at this period there is an extension of spectrum of ironcontaining enzymes with the heme structure that has begun to be the main structure for Fe-complexes in eukaryotes in the process of evolution. Thus, in the evolutionary hierarchy of ironcontaining compounds, which we have proposed (scheme I), in fundamental “blocks” of metabolism, it is possible to trace a transition from Fe(II)compounds in anaerobic processes to Fe(III)-complexes in aerobic ones, whose fine energy balance is associated with the Fe(II) : Fe(III) ratio and determines the cell biochemical state. We consider the hierarchy of iron compounds as a rise of their rank owing to internal rearrangements, particularly due to involvement of other ligands in the complexes at change of the degree of the metal oxidation. When considering the iron cycle at the biogeochemical level, there seems reasonable the concept of importance of the ratio of the iron concentration and the (II) and (III) oxidation states as an ecological factor that determines buffer capability in microzones at the phase boundary, under the so-called gradient conditions [10, 11] forming geochemical barriers. These barriers are peculiar “sites” of the earth crust, which have been used by Nature to model geochemical conditions (“situations”) with specific physical-chemical characteristics that provide a local concentration of some compounds: these are ecological habitation areas that are the most favorable for biogenesis. BIOGEOCHEMICAL CYCLE OF IRON Iron occupies the second place among metals and the fourth among elements by the per cent contents (4.65%) in the earth crust. Iron is an important bioelement, its per cent contents in the living matter amounts to 1 × 10–2%. The richest in natural iron deposits are the preCambrian oxidized sediments, known as blended irons formations (BIFs) that concentrate about 28% of the earth crust iron. They represent alternating layers of siliceous rock containing magne-

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tite and goethite [14]. These formations are of sea origin, their age is 3.2–1.9 bln years [15]. Other crystalline iron reserves are bog iron ores, ”red stratas”—continental or marginal deposits, in which fine grains of silicon dioxide are covered by iron oxides [15], and also hydrothermal deposits formed as a result of volcanic and magmatic activity, and iron–manganese deposits of lakes and oceans, but all of them are quantitatively less than BIFs. The biogeochemical iron cycle in nature is a complex of the global “slow” geochemical cycle and minor biological turnovers performed with partici pation of living organisms, mainly microorganisms. The main part of iron in the modern geosphere is in the oxidized state that is stable for this element under the most predominant aerobic conditions with the neutral and low-alkaline reaction. Therefore, the global iron cycle is a slow geological cycle characterized by disposals, metamorphoses, volcanism, weathering, and other physical-chemical mechanisms of transformation and transport. However, there are in the nature such conditions, in which the iron cycle proceeds rather fast. These are reductive or partly anaerobic zones, in which reduction of iron and its mobilization is observed. The examples of such zones are bottoms of eutrophized and stratified lakes, seasonal anaerobic ponds, partly anaerobic deposits of the marine and freshwater origin, moors, etc. In performance of stages of the “fast” iron cycle, the determining role is played by microorganisms interacting with iron of geological deposits at gradient geochemical barriers. Such microorganisms are believed to be the main partici pants of the BIFs formation [16]. Taking into account biochemical transformations of iron at the cellular level and biogeochemical processes of global geological cycle, the partici pation of bacteria in the iron turnover may be presented as follows (Scheme II). A link between the cellular and biogeochemical levels are Fe(III)compounds that predominate in nature and are low soluble at ðÍ > 3.0. Thus, concentration of Fe(III) ions of hydroxides in water amounts to around 10–17 M [19]. Prokaryotes have developed various mechanisms of the iron transport and

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Scheme II. Partici pation of bacteria in iron cycle [16–18]

Få(II) –Få(III)-complexes absorbed by cell

BIOMINERALIZATION (hydroxides, bacterioferritin, ferrihydrite, pyrrhothine, magnetite, gragite)

Siderophoric binding

BASAL METABOLISM (iron-containing enzymes)

Clearing at dying

Clearing at dying Fe(III)-compounds: oxides, hydroxides etc. (neutral conditions of medium)

Precipitation and sedimentation

Fe(III)-minerals, FeOOH, Fe2O3, Fe(OH)3

Fe(II) dissolution

Reduction

Fe(III) deposition

Fe3O4 Magnetite production

Oxidation Gragite production

Buried minerals

FeS deposition

Fe(II), Fe(III) metabolism

Fe3S4

Få(III) Fe-reduction (neutral conditions of medium)

S-oxidizing bacteria

Fe-oxidation (low pH of medium)

Få(II), H2SO4

B I O C H E M

P R O C E S I S C E A S L B I O G E O C H E M I C A L

P R O C E S S E S

Disposal and diagenesis

absorption to provide their metabolic needs in iron [20]. Many microorganisms are able to release siderophores into the environment; these form complexes at interaction with iron ions (siderophoric binding). By such a way the transport of iron into the bacterial cell is the most favorable. The Fe-ion absorbed as a result of the specific transport is used in basic processes of metabolism and in biogenesis (in some species). After dying, the cell and the iron-containing complexes formed by the cell enter the environment and are involved in the biogeochemical cycle. Besides, microor-

ganisms partici pate indirectly in transformation of iron compounds due to a release of mucus, formation of capsules and changes of extracellular ðÍ in the process of metabolism. This results in a passive deposition of several iron-containing minerals on the cell surface and in the environment [21]. At the biogeochemical level, of significance are processes of preci pitation, sedimentation, and Fe(II)/Fe(III) metabolism in microbial biocenoses. The closure of the biogeochemical cycle is provided by the Fe(II) oxidation and Fe(III) reduction, the disposal and diagenesis

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being possible). On biogeochemical barriers (gradients of alkaline-acidic and oxidation–reduction potentials), a partial reduction of Fe(III) with formation of magnetite is possible. In some cases, in such compounds there is an isomorphous substitution of oxygen by sulfur with formation of pyrrhothine (Fe1–xS, where õ varies from 0 up to 0.2) and gragite (Fe3S4). All these minerals have strong magnetism [22]. It is to be reminded that when considering biochemical processes of transformation of iron at the cellular level, we also should note the extraand intracellular formation of magnetite, pyrrothine, gragite, and some other minerals (scheme I). Apparently, there are common mechanisms of biogenesis of such minerals at the cellular level, and also as a result of interaction of abiogenic and biogenic pathways of formation of these minerals at the level of biogeochemical transformations. Comparing energy values (∆G0) of the dynamic system of magnetite formation with partici pation of bacteria under anaerobic conditions (1) and during weathering (2), a much higher efficiency of the first process can be noticed: (∆G0), kJ/mol ÑÍ3ÑÎΖ + 24 Fe(OH)3 = 8 Fe3O4 + ÍÑÎ3– + 37 H2O (–712) [ 23 ], (1) Fe2O3 + H2O + 2 e– = 2 Fe3O4 + 2 OH– (–442) [24]. (2)

The magnetite is considered in biomineralogy as a mineral that is spread sufficiently wide in living organisms [8], including human [25, 26], whereas under abiogenic conditions it is formed in metamorphic and magmatic deep rocks, scarns, as well as in middle- and high-temperature hydrothermal deposits, i.e., where there is a source of exogenous energy. It indicates once again an importance of mechanisms of biological induction and control of biogenesis of this mineral, which seem to have developed in the process of evolution. Besides, it is a perfect example of a strong interrelation of living organisms and the inert matter in the biogeosystem, when considering the concept of the iron cycle in nature. The basis of this interrelation is the energy transformation Fe(II) ↔ Fe(III) that determines turnover of biochemical energy both at the cellular and at the biogeosystemic levels and in the process of evolutionary biochemical adaptation.

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CONCLUSION The exposed above allows stating the key role of iron in the appearance and evolutionary development of the Earth and its biosphere. The role of this element may be expressed as the following hierarchical chain of historical transformation: metallic Fe (Earth core and mantle) → metallic Fe and FeO oxide in primordial regolith and volcanic ashes (a catalyst of synthesis of organic compounds) → Fe/Fe(II)-relation, where oxidation occurs at binding of O2 formed at photolysis of water → Fe(II)/Fe(III)-relation, where oxidation of Fe(II) in Fe(III) occurs by binding of O2 formed as a result of oxygenic photosynthesis by cyanobacteria → Fe(II) ↔ Fe(III) energy transformation that is the oxidation–reduction energy “core” of the most important metabolic iron complexes and processes of biogenesis both at the cellular level and in biogeosystems, which has determined the princi pal role of iron in nature. As a connecting link between these levels, magnetically arrayed minerals of iron may be considered, in which the element exists both in the Fe(II) and in the Fe(III) state. ACKNOWLEDGMENTS The work is supported by the program “Universities of Russia” (project no. 1169). REFERENCES 1. 2. 3.

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