evolutionary role of iron

0022-0930/01/3704-0444$25.00 © 2001 MAIK �Nauka/Interperiodica�

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 Prokaryotesand 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 ironin the appearance and evolutionary formation of the Earth and its biosphere. Participation of ironand its compounds in the appearance and development of processes of anaero- and aerobiosis asfundamental �blocks� of metabolism is presented as a hierarchical scheme. Magnetically arrayediron compounds, in which the element is both in the Fe(II) and in the Fe(III) state, are considereda 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 andof processes of biogenesis both at the cellular level and in biogeosystems.

IMPORTANCE OF IRON IN FORMATIONOF BIOSPHERE ON THE EARTH

According to modern concepts of some geolo-gists, geochemists, biochemists, and microbiol-ogists, the whole evolution of the Earth and pos-sibility of origin of life on it depended essentiallyon the ratio of Fe and FeO in the Earth crust [1�4], i.e., on the ratio of amounts of metallic ironand Fe(II), which in the primordial Earth mat-ter amounted to 13 and 24%, respectively. Inthe early Earth history these iron forms were themain absorbents of oxygen formed at photolysisof water, the metallic iron amount decreasing inthe 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 theform of Fe(II) compounds (for example, FeS-proteins and ferredoxin (EC 1.8.7.1)) as electroncarriers in strict heterotrophic anaerobic fermen-tators [5].

The subsequent accumulation of oxygen in at-mosphere (due to oxygenic photosynthesis by cy-anobacteria) was accompanied by its binding byFe(II) iron oxide and conversion to Fe(III).With the accumulation of free oxygen in the Earthatmosphere a shift to the next oxygenic stage oflife evolution, iron was included in metabolicpathways both in the Fe(II), and in Fe(III)state. The importance of such compounds is dueto ability of their �iron�oxide� core to acceptor release electrons in the course of transforma-tion Fe(II) ↔ Fe(III), which, thereby, is theenergy center. Participation in diverse oxidation�reduction reactions determines the essential im-portance of iron complexes both at the level ofmetabolic transformations in the cell, and in bio-geochemical processes. These levels are consid-ered 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 IRONTRANSFORMATIONS AT THE CELLULAR

LEVEL

The iron occupies a special place among 12macroelements necessary for the life activity ofboth prokaryotic, and eukaryotic organisms at arelatively high (> 10�4 M) concentration. Thesignificant role of iron in metabolism is due to itspeculiarity as a transient element that can easilychange its oxidation degree, Fe(II) or Fe(III).It allows iron to coordinate various electron do-nors (coordination ligands) and to participate invarious oxidation�reduction processes. Ligandsform various surrounding of the core, which de-termines formation of iron complexes, particu-larly, of iron-containing proteins, in nature.Owing to the wide occurrence, as well as to theirproperties, these compounds were included infundamental processes of metabolism in organ-isms: in DNA synthesis (ribonucleoside diphos-phate reductase (EC 1.17.4.1) and ribonucleosidetriphosphate reductase (EC 1.17.4.2)), in photo-synthesis, respiration, nitrogen fixation, and someothers [6]. At present, more than 20 of suchmetabolically important biocomplexes have beenknown. As compared with other metals (Mg,Ca, Co, Cu, Zn, Mo) forming metallobiomol-ecules in organisms, only iron forms such diver-sity of biocomplexes [7].

In the scheme I we have tried to present themain stages of evolution of biosphere, anaerobicand aerobic, and to specify fundamental process-es of life activity of prokaryotes and the proteiniron complexes that determine the occurrence ofthese processes.

Considering evolutionary development ofprokaryotes, bacteria and cyanobacteria, thatprevail on the Earth during more than 3 bln yearsand are �test objects of the Nature� in its searchfor optimal biochemical pathways of metabolism,a direct participation of iron compounds can benoted in this natural selection of metabolism. In-deed, protein complexes of iron participate in allfundamental processes of the life activity both atanaerobic, and at aerobic stages of evolution ofbiosphere (scheme I).

Thus, such �ancient� protein complexes ofiron, as FeS-proteins, ferredoxin, rubredoxin (EC

1.18.1.1), hydrogenase (EC 1.18.99.1), cyto-chrome c oxidase (EC 1.9.3.1), are involved inthe most important energy processes of anaerobi-osis, fermentation evolutionary more recent pho-tosynthesis in eubacteria. The same enzymes pro-vide anaerobic nitrogen fixation. The iron-con-taining enzymes are also necessary in anaerobicrespiration: �nitrate� and �sulfate�: nitrate reduc-tase (EC 1.7.99.4) and nitrite reductase (EC1.7.99.3), and hydrogenase, respectively. Besides,there are processes of biogenesis of iron compoundsat the anaerobic stage of life, i.e., extra- and in-tracellular formation of iron minerals with par-ticipation of bacteria. More than 10 such biom-inerals have been described [8]. Of a special in-terest is the ferrimagnetic mineral magnetite(FeO2 � Fe2O3) that is composed both of Fe(II),and of Fe(III), i.e., at the biochemical level thegradient (microaerobic) conditions occur, underwhich the energy balance in relation to the ironmineral formation is determined by the ratioFe(II) : Fe(III). The problem of the biomineral-ization process and the magnetite biogenesis is con-sidered below in a greater detail.

In the oxygen atmosphere, spectrum of ironcomplexes participating in metabolism of prokary-otes was extended, while Fe-enzymes of anaero-bic stage of the biosphere development were pre-served. By their example it is possible to follow�the evolution itself that looks like a gradual com-plication, whose previous stage is included in thesubsequent one as a necessary constituent� [9].Thus, the aerobic transport chain was composedof iron-containing dehydrogenases: succinate de-hydrogenase (EC 1.2.1.16), NADH dehydroge-nase (EC 1.6.99.2), formiate dehydrogenase (EC1.2.1.43), and cytochromes. The defense fromreaction oxygen compounds was required, so suchiron complexes as superoxide dismutase (EC1.15.1.1), xanthine oxidase (EC 1.2.3.2), cata-lase (EC 1.11.1.6), peroxidase (EC 1.11.1.7) were�selected� in the process of evolution to performthis task. Cofactor of the above-listed enzymes isiron with the (III) oxidation state, whose revers-ible reduction to Fe(II) determines their func-tioning. Besides, catalase and peroxidase containiron in the heme structure.

The oxygen stage of the nitrogen cycle, apartfrom Fe-enzymes participating in anaerobic ni-

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trogen fixation, includes leghemoglobin (EC1.6.2.6), providing oxygen binding and defense ofthe nitrogenase complex of symbiotic nitrogen fix-ers from its reaction action. As a whole, at thisperiod there is an extension of spectrum of iron-containing enzymes with the heme structure thathas begun to be the main structure for Fe-com-plexes in eukaryotes in the process of evolution.

Thus, in the evolutionary hierarchy of iron-containing compounds, which we have proposed(scheme I), in fundamental �blocks� of metabo-lism, it is possible to trace a transition from Fe(II)-compounds in anaerobic processes to Fe(III)-com-plexes in aerobic ones, whose fine energy balanceis associated with the Fe(II) : Fe(III) ratio anddetermines the cell biochemical state. We con-sider the hierarchy of iron compounds as a riseof their rank owing to internal rearrangements,particularly due to involvement of other ligandsin the complexes at change of the degree of themetal oxidation.

When considering the iron cycle at the bio-geochemical level, there seems reasonable theconcept of importance of the ratio of the ironconcentration and the (II) and (III) oxidationstates as an ecological factor that determines buffercapability in microzones at the phase boundary,under the so-called gradient conditions [10, 11]forming geochemical barriers. These barriers arepeculiar �sites� of the earth crust, which havebeen used by Nature to model geochemical con-ditions (�situations�) with specific physical-chem-ical characteristics that provide a local concen-tration of some compounds: these are ecologicalhabitation areas that are the most favorable forbiogenesis.

BIOGEOCHEMICAL CYCLE OF IRON

Iron occupies the second place among metalsand the fourth among elements by the per centcontents (4.65%) in the earth crust. Iron is animportant bioelement, its per cent contents inthe living matter amounts to 1 × 10�2%.

The richest in natural iron deposits are the pre-Cambrian oxidized sediments, known as blendedirons formations (BIFs) that concentrate about28% of the earth crust iron. They represent alter-nating layers of siliceous rock containing magne-

tite and goethite [14]. These formations are ofsea 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 coveredby iron oxides [15], and also hydrothermal de-posits formed as a result of volcanic and mag-matic activity, and iron�manganese deposits oflakes and oceans, but all of them are quantita-tively less than BIFs.

The biogeochemical iron cycle in nature is acomplex of the global �slow� geochemical cycleand minor biological turnovers performed withparticipation of living organisms, mainly micro-organisms. The main part of iron in the moderngeosphere is in the oxidized state that is stable forthis element under the most predominant aerobicconditions with the neutral and low-alkaline re-action. Therefore, the global iron cycle is a slowgeological cycle characterized by disposals, meta-morphoses, volcanism, weathering, and otherphysical-chemical mechanisms of transformationand transport.

However, there are in the nature such condi-tions, in which the iron cycle proceeds ratherfast. These are reductive or partly anaerobiczones, in which reduction of iron and its mobili-zation is observed. The examples of such zonesare bottoms of eutrophized and stratified lakes,seasonal anaerobic ponds, partly anaerobic de-posits of the marine and freshwater origin, moors,etc.

In performance of stages of the �fast� iron cy-cle, the determining role is played by microor-ganisms interacting with iron of geological depos-its at gradient geochemical barriers. Such micro-organisms are believed to be the main participantsof the BIFs formation [16].

Taking into account biochemical transforma-tions of iron at the cellular level and biogeochem-ical processes of global geological cycle, the par-ticipation of bacteria in the iron turnover may bepresented as follows (Scheme II). A link betweenthe cellular and biogeochemical levels are Fe(III)-compounds that predominate in nature and arelow soluble at ðÍ > 3.0. Thus, concentration ofFe(III) ions of hydroxides in water amounts toaround 10�17 M [19]. Prokaryotes have devel-oped various mechanisms of the iron transport and

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absorption to provide their metabolic needs in iron[20]. Many microorganisms are able to releasesiderophores into the environment; these formcomplexes at interaction with iron ions (sidero-phoric binding). By such a way the transport ofiron into the bacterial cell is the most favorable.The Fe-ion absorbed as a result of the specifictransport is used in basic processes of metabolismand in biogenesis (in some species). After dying,the cell and the iron-containing complexes formedby the cell enter the environment and are involvedin the biogeochemical cycle. Besides, microor-

ganisms participate indirectly in transformation ofiron compounds due to a release of mucus, for-mation of capsules and changes of extracellularðÍ in the process of metabolism. This results ina passive deposition of several iron-containingminerals on the cell surface and in the environ-ment [21]. At the biogeochemical level, of sig-nificance are processes of precipitation, sedimen-tation, and Fe(II)/Fe(III) metabolism in micro-bial biocenoses. The closure of the biogeochemi-cal cycle is provided by the Fe(II) oxidation andFe(III) reduction, the disposal and diagenesis

Scheme II. Participation of bacteria in iron cycle [16�18]

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

BIOMINERALIZATION(hydroxides, bacterioferritin, ferrihydrite,

pyrrhothine, magnetite, gragite)

Clearing at dying

Precipitation and sedimentation

Fe(III)-compounds:oxides, hydroxides etc.

(neutral conditions of medium) Fe(II), Fe(III)metabolism

Fe(II) dissolution

Fe(III) deposition

Fe O3 4Fe(III)-minerals,

FeOOH, Fe O , Fe(OH)2 3 3Magnetite production

Gragite production Fe3 4S

OxidationReduction

FeS deposition

Fe-reduction (neutral

conditionsof medium)

Buried mineralsS-oxidizing bacteria

Disposal and diagenesis

Få(II), H SO2 4

Få(III)

Fe-oxidation (low pH of medium)

Clearing at dying

BASAL METABOLISM(iron-containing enzymes)Siderophoric binding

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being possible). On biogeochemical barriers (gra-dients of alkaline-acidic and oxidation�reductionpotentials), a partial reduction of Fe(III) withformation of magnetite is possible. In some cas-es, in such compounds there is an isomorphoussubstitution of oxygen by sulfur with formation ofpyrrhothine (Fe1�xS, where õ varies from 0 upto 0.2) and gragite (Fe3S4). All these mineralshave strong magnetism [22].

It is to be reminded that when considering bio-chemical processes of transformation of iron atthe cellular level, we also should note the extra-and intracellular formation of magnetite, pyrroth-ine, gragite, and some other minerals (scheme I).Apparently, there are common mechanisms ofbiogenesis of such minerals at the cellular level,and also as a result of interaction of abiogenicand biogenic pathways of formation of these min-erals at the level of biogeochemical transforma-tions. Comparing energy values (∆G0) of the dy-namic system of magnetite formation with partic-ipation of bacteria under anaerobic conditions(1) and during weathering (2), a much higherefficiency of the first process can be noticed:

(∆G0), kJ/molÑÍ3ÑÎÎ� + 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 asa mineral that is spread sufficiently wide in livingorganisms [8], including human [25, 26], whereasunder abiogenic conditions it is formed in meta-morphic and magmatic deep rocks, scarns, as wellas in middle- and high-temperature hydrothermaldeposits, i.e., where there is a source of exogenousenergy. It indicates once again an importance ofmechanisms of biological induction and control ofbiogenesis of this mineral, which seem to have de-veloped in the process of evolution. Besides, it is aperfect example of a strong interrelation of livingorganisms and the inert matter in the biogeosys-tem, when considering the concept of the iron cy-cle in nature. The basis of this interrelation is theenergy transformation Fe(II) ↔ Fe(III) that deter-mines turnover of biochemical energy both at thecellular and at the biogeosystemic levels and in theprocess of evolutionary biochemical adaptation.

CONCLUSION

The exposed above allows stating the key roleof iron in the appearance and evolutionary devel-opment of the Earth and its biosphere. The roleof this element may be expressed as the followinghierarchical chain of historical transformation:metallic Fe (Earth core and mantle) → metallicFe and FeO oxide in primordial regolith and vol-canic ashes (a catalyst of synthesis of organic com-pounds) → Fe/Fe(II)-relation, where oxidationoccurs at binding of O2 formed at photolysis ofwater → Fe(II)/Fe(III)-relation, where oxida-tion of Fe(II) in Fe(III) occurs by binding of O2formed as a result of oxygenic photosynthesis bycyanobacteria → Fe(II) ↔ Fe(III) energy trans-formation that is the oxidation�reduction energy�core� of the most important metabolic iron com-plexes and processes of biogenesis both at the cel-lular level and in biogeosystems, which has de-termined the principal role of iron in nature. Asa connecting link between these levels, magneti-cally 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 �Univer-sities of Russia� (project no. 1169).

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evolutionary role of iron

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