Metal is essential to metabolic process in human life, for example photosynthesis , nitrogen fixation and aerobic respiration. According to the percentage the elements making up of most organisms, elements can be crudely classified into either bulk or trace elements. Transition metals which make up less than 0.1 % are trace elements. With its low bioavailability in organisms, its main function includes: electron transfer agents, structural formation in metalloproteins, delivery of reactants to the active site1. Due to the important function played by metal, it may serve as a driving force in the evolution of life on earth2. Due to the physical chemistry properties of metal like redox/oxidate potential and precipitation in certain chemical environment which is closely related to the bioavailabity of metals. Based on this idea, the availability of metal is directly associated with geochemistry of ocean and atmosphere. Thus metal may be a key bridge in associating the evolution with the environment through a more interactive way. A general overview of metals in ocean through the 4-billion-year history of life on Earth is outlined below first for later detailed discussion. It is generally accepted that the ocean is anoxygenated during the Archean( time before the 2.5 Ga). The anoxic and reducing Archean ocean would have been enriched in ,,and ,yet low in ,,and .The following emerging of oxygenic photosynthesis and the resulting increase in atmospheric levels around 2.4 Ga, promoted a transition to a euxinic(anoxic and sulfidic) Proterozoic ocean caused by continental weathering and oceanic sulfate reduction. In this euxinci ocean, ,and concentrations would have decreased yet remained high concentration comparing to the modern ocean ,whereas and would have declined several orders of magnitude. Later the transition to a generally oxidizing ocean () resulted in a large increase in,,and,with concomitant decrease in ,,and ,accompanied with the burst of life in forming the vibrant and diverse of species earth. A figure is shown below describing the metal concentration in ocean and oxygen in atmosphere through the history2(Figure 5).
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The early evolution(3.8Ga-around 2.4Ga)
It is assumed that the Sun and earth formed around 4.6 billion years ago, but suggested by isotopic data that accumulation of liquid water on the earth did not start after 200 million years of the formation of earth3. There is still debate about the constitution of early atmosphere. Some suggest that early atmosphere was a hydrogen rich earth, consisting of ,,,4, which is different to today's atmosphere. Modern atmosphere is made up of ,,,,which is key to all the living system of the earth. Generally most people think it is certain that life began at least 3.5 GA before and it is probable that life is present 3.8 GA or even earlier. However, at that time, the environment for the origin of life is still tough. Temperature though had cooled down ,but still could reach up to 100 â„ƒ due to frequent impacting bodies on the exterior. 5Under the chaotic condition of surface of ocean, the warm springs in the deep sea were a good choice for the origin of life. It provided not only consistency of PH and temperature, but also raw materials that were crucial6. The volcano eruptions provided enough hot-dissolved minerals including: manganese, iron, sulfide, phosphate, nickel, cobalt and zinc which is crucial to the evolution of life5. However the first life still faced serious problem, it had to bear the high temperature up 100 â„ƒ or it won't survive the hit of meteorite. The universal ancestor is considered hyperthermophiles though some consider it not the only ancestor7. During the period the light was not reachable to the deep sea, because of the impact of meteorite and the so-called "black smokers" which shade the light. Still life needed energy to survive before the emerging of photosynthesis. In this period, we will mainly focus on the energy metabolism of hyperthermophiles. The mode of energy metabolism of hyperthermophiles are diverse, but are mainly based on the oxidation of or coupled the reduction of ,,and ,but rarely use .Several metabolism pathways have been revealed.(Table 1)8. Molecular hydrogen is contributed by a geochemical process at early stage. Exergonic formation of pyrite ()from and
Energy metabolism usually is coupled with the synthesis of ATP as the energy source through the mechanism of electron transport phosphorylation. The usual pattern for the metabolism of energy present as : First hydrogen or carbon monoxide is oxidized via hydrogenase. Then electron flow to inorganic electron acceptors and at the same time ATP is synthesized through ATP synthase.8 Tough organic cofactors able to transport protons evolved early before the use of metal through coordination structure, redox transformation was possible until when coupled with metal binding electron transport proteins. Evidence show that the earliest evolving ,andbinding protein are involved in electron transfer and the transformations of ,,and10. According to Günter Wächtershäuser, we can infer from four aspects to deduce the origin of life. As to the source of carbon atoms, fixation is the main pathway. and are both possible candidates for the pathway. The emphasis has shifted from to , due to its highly reactivity and has three central biological functions11. As to the source of reducing power, see the table summarized the sources of electrons (Table 2)11.As to the source of sulphur, volcanic is the essential source for 'ancestor organism'. Finally, as to many early biological function, transition metal centre of inorganic substructure is important, Which is what we will focus on in this review. It is suggested that metals including ,,,,,,,andligands combine to a rich set of possible inorganic structures on mineral surface or precipitation of minerals12. Several reactions involving minerals which have been experimentally tested emphasize the role metal played in the origin stage of evolution.(Table 3)11. Not only simple chemical reactions that provide energy use metal or mineral as reaction biological centre , but also synthesis of low-molecular compounds reactions are catalyzed by metal centre in or on the surface of minerals. Some of these synthesis have been revealed.(Table 4)11.
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A notable feature for these energy and carbon fixation metabolisms is that most of them are carried out based on enzymes using metal as centre for catalysis. Structures like,, are widely used in various enzymes before the great oxidation event(GOE). An specific example of hydrogenase is used to show more details about those metals as catalytic centre. Hydrogenases were important in the early stage when hydrogen dominated the atmosphere and were available in the ocean from crust activity and volcano eruptions, with hydrogen being used as main energy vector. There are at least three kinds well-studied Hydrogenases: , and hydrogenases. The main function of the three hydrogenases are listed below (Table 5)13. Though phylogenetically unrelated, active sites in the three hydrogenase contains a unit, with in hydrogenase and in and hydrogenase. Also one or two iron ions in and hydrogenases are all bounded by two ligands, respectively14. In hydrogenase , the active-site iron is bounded with a guanylylpyridinol cofactor through an sp2-hybridized nitrogen and a formyl carbon atom15. In hydrogenases, two bridging and two nikel-binding terminal Cys thiolates maintain the coordination of the hydrogenase16. Inhydrogenases, the active site is an known 'H-cluster' unit. While the subunit is bounded with a Cys thiolate and a five-five atom dithiolate ligand with the bridgehead unknown limited by the resolution(x in Fig.1a). Crystal structure of the three hydrogenase show vacant ligand sites which are potentially for substrate binding with the catalytic metal. In and hydrogenases the metal catalytic centre will form a complete an octahedral coordination sphere if binds to the one vacant site. Two vacant sites including a terminal and a bridging coordination sites are available for substrate binding in [NiFe]-hydrogenases to complete an octahedral coordination13.
Possible catalytic mechanisms for the enzymes discussed above are presented in Fig. 2. The and hydrogenases carry out reactions to catalyze molecular hydrogen to protons and electrons (Table 5, reaction 1a,1b,1c). However, hydrogenases catalyzed only the first step (Table 5, reaction 1a) and then carry out reaction 1b14. The active site of iron ion in and hydrogenases is binding with high-field, acceptor and , making it a relatively soft Lewis acid. This in turn , favors its binding to the soft Lewis base .This leads to a probable step in the catalysis (Table 5,reaction 1a).The direction of the reaction in and hydrogenases is affected by the redox and oxide state , the PH, the hydrogen concentration14. Fig 2a shows the two possible mechanism promoting two hydrogen-binding states of the active site of hydrogenase: ,product of the reductive activation(blued cycle); state, shown in equilibrium with .In both cycles we can see the change of valence state of nickel iron17. In hydrogenase , one of the ligand is thought to play as the role of switch between terminal and bridging positions ,according to the redox state of the metal centre18. Except active site in hydrogenase which is buried in the large subunit , active sites for the other two hyrogenases are located at or near the surface of the protein . Apart from the hydrogenese , studied enzymes have tunnels which are mainly hydrophobic to transfer gaseous substrate or product in the protein . This promote the reaction and concentration of hydrogen in the protein 13. It is notable that in the early stage, metal played various roles in catalysis and structural roles in energy metabolism and life growth(carbon fixation and nitrogen fixation), which is crucial in shaping the early atmosphere and the later evolution of life on earth.
The evolution of photosynthesis(Example 1)
As mentioned above, after the origin of life on earth around thermal vents utilizing minerals as catalyzing core to oxidize substrates like ,,,and as source of energy. Among which was probably the most important19. When the conditions of the earth and primitive sea became mild, the lives also spread to places not only restricted to hot spring. Primitive phototrophs which thought to have performed simple anaerobic photosynthetic processes emerge in the Archean period of earth. Though in the early period ,these anoxygenic photographs cannot oxidize water and produce molecular oxygen . They mainly use the reducing materials which is present in high concentrations, and change the environment of the primitive sea(Table 6)20. Finally pave the way for the emergence of aerobic photosynthetic, and result in the Great Oxidation Event around 2.4 billion years ago.
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Tough difficult to prove to the exact time of the evolving of photosynthetic organisms ,it is widely accepted that they were present before 3.5 billion years ago21. These organisms use bacteriochlorophylls to absorb photons. Light excitation results in the transfer of electrons from an excited donor molecule to a series of electron acceptors in pigment-protein complexes. One of the key components in photosystem is the photosynthetic pigment. Little doubt has been proposed that the first effective photosynthetic pigments were Mg-porphyrins, such as Mg-protoporphyrin monomethyl ester. It is shown that the chelation of at this stage that distinguishes this line of development from that of heme formation where is involved22. The structure of the pigment will determine the region of spectrum of the Sun it uses. For the early microbes in the deep sea, the pigment mainly takes in the light in the ultraviolet and blue spectrum. The later emerging of aerobic photosynthesis takes advantage of the part of the Sun's spectrum with higher energy: mainly in the region of visible light23. Between 2.4 Billion years ago to 0.5 billion years ago the great increase of oxygen in the atmosphere, the aerobic photosynthesis prevailed and tended to occupy the surface of ocean. Thus the anaerobic photosynthesis can only refugia to where: 1)oxygen was restricted; 2) where reducing conditions were available (,,organic compounds); 3)where the light climate was likely to be stripped of visible light by cynobacteria and/or water-quality effects24. The structure of chlorophylls and Bacteriochlorophylls used in aerobic and anaerobic photosynthesis respectively are shown in figure 3.
After light harvesting systems capture the energy of photons from the Sun, the light excitation results in the electron transferring from a primary electron donor to a quinine serving as the secondary electron acceptor through a series of intermediate cofactors. For the bacteria reaction centre of different bacteria they are just slightly different in structure. Here we will present bacteria reaction centre of purple bacteria as an example. We will compare the bacteria reaction centre with the later involving photosystem â…¡ to see the evolution of photosynthesis. For photosystem â…¡ and the reaction centre , the binding site of the secondary quinine and electron transfer processes are highly similar. However, the oxidizing sides are distinctive. Either an exogenous cytochrome that binds to the reaction centre or a bound cytochrome reduce the primary donor P856 from purple bacteria, transfer an electron. In photosystem â…¡, the primary donor P680, is rapidly reduced by the amino acid cofactor, . The forming neutral tyrosyl radical then is reduced by the cluster. After collecting four-electron equivalents,molecular oxygen is generated through the oxidation of two water molecules bound to the cluster25. Instead of oxidizing reducing material, the evolving photosystem â…¡ have the amazing property to oxidize water which is very stable . In order to oxidize water, a midpoint potential greater than +0.82 V at PH 7 is needed. The midpoint potential of P680 is about 1.1-1.4 V, making P680 the strongest known biological oxidant26. However, with only a moderate midpoint potential of 0.5 V and thus, P865 cannot oxidize water or tyrosine, only species of lower potential like the heme of cytochrome (Table 6)27. While reasons that give rise to the difference in midpoint potential between P680 and P865 have not been specifically identified, dissimilarities of the donors from the environment in the two complexes may account for the difference in midpoint potential. Also the differences in structures and properties of BChl(Bacteriochlorophyll monomer) and Chl(Chlorophyll) contribute part to the difference in midpoint potential which have already been mentioned in figure 3. This difference in structure is also responsible for the absorption of Chl at a shorter wavelength of 680 nm compared to 865 nm of BChl , making the energy available for photosystem â…¡ much higher at 1.82 eV compared to 1.2 eV for bacteria centre25. Thermodynamic calculation suggests that this amount of light energy is necessary to generate the highly oxidizing28. Studies in mutation of the reaction centre show that the initial incorporation of Chl rather than BChl would have increased the midpoint potential of the primary donor to a point where the complex could perform new photochemistry, namely the oxidation of a manganese ion in the Oxygen-Evolving Centre (OEC) which will be discussed below. Experiments show that the achievement of subsequently increasing high potential found in photosystem â…¡ could have been achieved through amino acid alterations29.
The anoxygenic bacteria use either RC(Reaction Centre)â… , or a prototype of RC â…¡ ,depending on species and environment . Cyanobacteria use the oxygenic PS(Photosystem) â…¡ and PSâ… electron transport system as dose algae and plants. The original RCâ… operates with external reductants, such as hydrogen sulfide, and is capable of supplying electrons to a quinine pool, which can then recycle the energized electrons back to the reaction centre while moving prontons across the membrane into the periplamic space thereby creating a protomotive force for the synthesis of ATP30. Over time and changing conditions, suitable electron donors (,, organic compounds) were used up on the early earth. The selective pressure force the oxidizing end of original RCâ… to change to more oxidizing reduction potential values, extending the oxidizing range of intermediate compounds and finally able to utilized to oxidize water. As discussed by Larkam24, three proposals have been put forward regarding compounds which may have been served as precursors to the manganese complex.(1)formate (2)hydrogen peroxide(3)bicarbonate. While bicarbonate is an ideal precursor because of its abundance in the early oceans due to the much higher levels of carbon dioxide existed then. Other evidence shows that bicarbonate is associated with the water oxidizing site, as well as bicarbonic anhydrase activity found in association with PS â…¡.
Once a highly oxidizing complex evolved, a metal cluster is also required for water splitting in order to store the four-electron equivalents needed for the reaction. In photosystemâ…¡,this cofactor is a cluster containing four and one ,known as Oxygen-Evolving Centre(OEC)31(Figure 6). Despite the availability of the three-dimensional structure of photosystem â…¡, the precise arrangement of the remains undetermined as the co factors and its binding site are poorly resolved in the models. Tough, the data from X-ray spectroscopy don't determine the configuration, they do limit the possibilities. In order to store the electron equivalents, the cluster will undergoes a series of changes in its oxidation state. Electron paramagnetic resonance has helped establish the specific oxidation states of the .Although they are not firmly established for all of the S states(PSII reaction center cycles through a set of 5 oxidation states), the S2 state most likely has an electronic state with one(â…¢) and three(â…£)32. Given the complexity of the water oxidation, it is unlikely that a phototroph capable of water oxidation could suddenly emerge with simpler complexes arising only later as adaptations in restrictive environment. Some mimic the original reaction centre using mononuclear (â…¡) or (â…¡) . They find it able to reduce after light excitation33. The results shows with a minimal change of the reaction centre to bind a reductive active, it is possible to serve as an efficient secondary electron donor to. However it is difficult to envision how a mononuclear metal could store the four-electron equivalents needed for water oxidation. So, a multi-nuclear metal cluster is preferred to catalyze the reaction. A logical step after the mononuclear cluster in evolutionary development would have been a dinuclear cluster and finally lead to the cluster. It is suggested that a metal binding site may have been developed initially for a low potential metal such as and later adapted to after the donor become highly oxidizing, through either binding of Chl instead of BChl or a series of small assistive changes to the surrounding protein. The subsequent binding of a cluster, perhaps initially a mineral in solution that bound at the same site would have provided with the primitive complex with a new class of secondary electron donors, reactive oxygen species. Formation of such a cluster may have arisen through the binding of two clusters that initially were identical but later involved into a more efficient cluster with four chemically distinct 25. In the revolutionary process, the selection of rather than another metal would have occurred based on a number of considerations34. is one of the most abundant elements and the third in transition metals. During Archean period , the metal would have been most likely present in the form of complexes such as (â…¡)-bicabonate clusters. In addition to being stable and soluble, has the advantage of owning a wide range of oxidation states, typically being (â…¡) to (â…£).
The evolution of nitrogen fixation(Example 2)
It is know that nitrogen is another necessary element in life. However in atmosphere the most abundant nitrogen source is nitrogen gas which is also nonreactive. Until with no other option will the organisms choose to take up dissolved as their source of nitrogen. is the most biological accessible nitrogen source for living organisms for it is already in chemical form useful for biomolecules. However the concentration of is extremely low in the present-day ocean and is easily converted to other forms of nitrogen by oxidation and other processes. Others may be used as a source of N include: ,, dissolved organic nitrogen (,Urea and amino acid is the most common constitutes)35. In the evolution of pathways for nitrogen fixation, corresponding enzymes use transitional metals including: ,,, for catalytic use. The change of nitrogen source and the emerging of oxygen on the earth affect the evolution of the nitrogen fixation and the choice of the catalytic metal centre.
In the Archean anoxic sea, Oxygen was scarce in the atmosphere and ocean. Even then the vast majority of nitrogen in the oceans and atmosphere was present in the form of which is not bioavailable. Due to abiotic fixation, for example iron-sulfide minerals likely fixed some into at hydrothermal vents or some was fixed by lighting. It is reasonable to hypothesize that both and were present in the Archean oceans and the first enzymes to evolve were those involve in and assimilation36: nitrite reductase(NiR) and glutamine synthetase (GS)/glutamate synthase(GltS(BD)). Gentic sequence and protein structure of these enzymes are highly conserved across all photoautotrophs, supporting their great antiquity37. The early requirement for NiR and GltS(BD) is consistent with the metal biovailability in Archean oceans(Figure 4).It is also clear that and that exist in later enzymes in nitrogen fixation are absent from NiR and GltS(BD), consistent with accumulating evidence of very low concentration of these metals in the Archean ocean38. However and from abiotic production was probably not rapid enough to support a biosphere comparable to today's, which create a selection pressure favoring the evolution of biological fixation pathways39. Fossil and phylogenetic evidence suggests that some of cyanobacteria had acquired the ability to fix by the early Paleoproterozoic40. There exist three forms of nitrogenase using different metals (,and), which has led to the suggestions that Anf(the Fe-Fe nitrogennase) evolved in the Archean, when Fe was plentiful but Mo and V were scarce. However Anf is the least effective nitrogenase of the three, but is the most effective in the production of hydrogen. So it is suggested that Anf initially evolved for hydrogen production and later adopted for nitrogen fixation41.
There is few dispute that by 2.3 Ga, in the atmosphere rose above PAL. Though the rise of photosynthesis may have begun by 2.7 Ga, the reason for the delay of at least 300 Myr between the origin of oxygenic photosynthesis and the oxygenation of the environment is unclear42. One of the reasons contributes to it is the weathering reactions with iron sulfide (pyrite) and other reduced minerals including Mo and other bioessential metals. Due to the availability of mobilized Mo in the form of , is first time be used in the N-fixation enzymes such as Nif (nitrogenase) and nitrate reductase. The key advantage of Mo is that Nif is times more efficient at fixation in vivo than the alternative forms of nitrogenase43. Due to the availability of both Mo and Fe, organisms may have facilitated the incorporation of Mo at the enzyme active site while still maintaining heavy dependence on Fe for the rest of the Fe-S clusters.All three sets of genes are possessed by numerous microbes, like methanogenic Archean and anoxygenic photosynthetic Bacteria (predecessors of cyanobacteria), allowing them to inhabit in both high- and low- Mo environment44. It is interesting to notice that Anf in some anoxygenic photoautotrophs can incorporate a Mo-Fe cofactor when Mo is available which indicates the flexible in metal use of the organisms to survive the environment which is variable in Fe and Mo availability.
The GOE around 2.3 Ga led to the generation of in deep ocean waters. The sulfide in the deep water would have promoted the removal of and thus limiting the accumulation of Mo in the oceans despite the oxic continental weathering reaction in the surface of the sea. Under the same condition, the precipitation of Fe also resulted in a crash of concentration comparing to Archean ocean. Under these conditions,-fixing prokaryote would have struggled to obtain sufficient Mo and Fe for Nif and Anf19. Plylogenetic evidence suggests that eukaryotic nitrate reductase(NR) arose soon after the origin of eukaryotes in the late Archean. The Mo requirement of eukaryotic nitrate reductase (NR) is higher than that of the cyanobacteria Narb enzyme, eukaryotic growth may have been N-limited in the Mesoproterozoic ocean before the major increase of especially because eukaryoutes lack the ability to directly utilize 45. This limitation of of eukaryote proliferation fit well with the fossil record of algae which displays a radiation of green algae in the Cambrian46. Finally when marine life reach the oxygenation of the deep sea between the condition is led to a high Mo and low Fe concentration. Evidence show that modern algae can subsist on lower Fe quotas than cyanobacteria which may due to a more effective take-up and function system for N-fixation, and may partially explain the success of algae in the modern ocean36.
With the advent of large-scale sequencing, genomic studies using 3-D protein structures can help to elucidate the influence of trace metal on the evolution of macromolecule protein. Recent phylogenomic analysis of metalloprotein provide new information on the biological metal utilization through evolution10,47. Overall comparison of the sum of all metal-binding domains and proteome size indicates that the overall gain and loss of metal-binding domains is a fundamental and constant rate for all of life and the general direction is the metal-binding proportion of a proteome increases with expansions in proteome size. Accordingly metal is necessary in the evolution of proteome and life. In the Archean ocean the majority of the emerging protein structure bind metals abundant and they tend to utilize more than one metal. The Cambialistic metal-binding protein evolved earlier than metal specific counterparts.. ,and is preferred before the Great Oxidation Event (GOE) according to analysis and can correspond to the geochemical availability of metal, while in contrast and utilization evolved after the GOE when these metals were at least available in certain environment. The early evolution of containing structures and delayed emergence of structures binding directly using amino acid side chains, further support the conclusion. This characteristic of cambialistic metal-binding trend from promiscuity to specificity corresponds to observed general patterns in evolution of modern metalbolism48. The early turning to cambialism is mainly based on bioavailability and through later evolution the adaptations of structure and more suitable metal according to its need through a economical way may lead to efficiency in functionality like the example in nitrogen fixation and photosynthesis we have discussed in the previous chapters.
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