Evolution of metal ions in biological systems refers to the incorporation of metallic ions into living organisms and how it has changed over time. Metal ions have been associated with biological systems for billions of years, but only in the last century have scientists began to truly appreciate the scale of their influence. Major (iron, copper, manganese, magnesium, calcium, and zinc) and minor (cobalt, nickel, molybdenum, tungsten, vanadium, and early lanthanides) metal ions have become aligned with living organisms through the interplay of biogeochemical weathering and metabolic pathways involving the products of that weathering. The associated complexes have evolved over time.
Natural development of chemicals and elements challenged organisms to adapt or die. Current organisms require redox reactions to induce metabolism and other life processes. Metals have a tendency to lose electrons and are important for redox reactions. Metals have become so central to cellular function that the collection of metal-binding proteins (referred to as the metallomes) accounts for over 30% of all proteins in the cell. Metals are known to be involved in over 40% of enzymatic reactions, and metal-binding proteins carry out at least one step in almost all biological pathways.Metals are also toxic so a balance must be acquired to regulate where the metals are in an organism as well as in what quantities. Many organisms have flexible systems in which they can exchange one metal for another if one is scarce. Metals in this discussion are naturally occurring elements that have a tendency to undergo oxidation. Vanadium, molybdenum, cobalt, copper, chromium, iron, manganese, nickel, and zinc are deemed essential because without them biological function is impaired.
Origins
The Earth began as an iron aquatic world with low oxygen. The Great Oxygenation Event occurred approximately 2.4 Ga (billion years ago) as cyanobacteria and photosynthetic life induced the presence of dioxygen in the planet's atmosphere. Iron became insoluble (as did other metals) and scarce while other metals became soluble. Sulfur was a very important element during this time. Once oxygen was released into the environment, sulfates made metals more soluble and released those metals into the environment; especially into the water. Incorporation of metals perhaps combatted oxidative stress.
The central chemistry of all these cells has to be reductive in order that the synthesis of the required chemicals, especially biopolymers, is possible. The different anaerobic, autocatalysed, reductive, metabolic pathways seen in the earliest known cells developed in separate energised vesicles, protocells, where they were produced cooperatively with certain bases of the nucleic acids.
Hypotheses proposed for how elements became essential is their relative quantity in the environment as life formed. This has produced research on the origin of life; for instance, Orgel and Crick hypothesized that life was extraterrestrial due to the alleged low abundance of molybdenum on early Earth (it is now suspected that there were larger quantities than previously thought). Another example is life forming around thermal vents based on the availability of zinc and sulfur. In conjunction with this theory is that life evolved as chemoautotrophs. Therefore, life occurred around metals and not in response to their presence. Some evidence for this theory is that inorganic matter has self-contained attributes that life adopted as shown by life's compartmentalization. Other evidence includes the ready binding of metals by artificial proteins without evolutionary history.
Importance of metal ions in evolution
Catalysis
Redox catalysts The prebiotic chemistry of life had to be reductive in order to obtain, e.g. Carbon monoxide (CO) and Hydrogen cyanide (HCN) from existing CO2 and N2 in the atmosphere. CO and HCN were precursor molecules of the essential biomolecules, proteins, lipids, nucleotides and sugars. However, atmospheric oxygen levels increased considerably, and it was then necessary for cells to have control over the reduction and oxidation of such small molecules in order to build and break down cells when necessary, without the inevitable oxidation (breaking down) of everything. Transition metal ions, due to their multiple oxidation states, were the only elements capable of controlling the oxidation states of such molecules, and thus were selected for.
Condensation and hydrolysis O-donors such as HPO were abundant in the prebiotic atmosphere. Metal ion binding to such O-donors was required to build the biological polymers, since the bond is generally weak, it can catalyze the required reaction and dissociate after (i.e. Mg2+ in DNA synthesis).
Abundance of metals in seawater Element Prebiotic conditions (M) Aerobic conditions (M) Mg2+ ~ 10−2 ~ 10−2 Mn2+ ~ 10−6 ~ 10−8 Fe ~ 10−7 [Fe(II)] ~ 10−19 [Fe(III)] Co2+ ~ 10−9 ~ 10−9 Ni2+ < 10−9 < 10−9 Cu < 10−20 (very low) [Cu(I)] < 10−10 [Cu(II)] Zn2+ < 10−12 (very low) ~ 10−8 Mo ~ 10−9 (MoS, Mo(OH)6) 10−8 (MoO) W WS 10−9 (WO) H+ low pH (5.5?) pH 8.5 H2S 10−2 (High) low [SO (10−2)] O2 < 10−6 atm ~ 10−1 atm (21%)
Prebiotic (anaerobic) conditions
Around 4 Ga, the acidic seawater contained high amounts of H2S and thus created a reducing environment with a potential of around −0.2 V. So any element that had a large negative value with respect to the reduction potential of the environment was available in its free ionic form and can subsequently be incorporated into cells, i.e. Mg2+ has a reduction potential of −2.372 V and was available in its ionic form at that time.
Aerobic conditions
Around 2 Ga, an increase in atmospheric oxygen levels took place, causing an oxidation of H2S in the surroundings and an increase in the pH of the sea water. The resulting environment had become more oxidizing and thus allowed the later incorporation of the heavier metals such as copper and zinc.
Irving–Williams series
Another factor affecting the availability of metal ions was their solubilities with H2S. Hydrogen sulfide was abundant in the early sea giving rise to H2S in the prebiotic acidic conditions and HS− in the neutral (pH = 7.0) conditions. In the series of metal sulfides, insolubility increases at neutral pH following the Irving–Williams series: Mn(II) < Fe(II) < Co(II) ≤ Ni(II) < Cu(II) > Zn(II)
So in high amounts of H2S, which was the prebiotic condition, only Fe was most prominently available in its ionic form due to its low insolubility with sulfides. The increasing oxidation of H2S into SO leads to the later release of Co+2, Ni+2, Cu+2, and Zn+2 since all of their sulfates are soluble.
Metal ions
Magnesium Magnesium is the eighth most abundant element on earth. It is the fourth most abundant element in vertebrates and the most abundant divalent cation within cells. The most available form of magnesium (Mg2+) for living organisms can be found in the hydrosphere. The concentration of Mg2+ in seawater is around 55 mM. Mg2+ is readily available to cells during early evolution due to its high solubility in water. Other transition metals like calcium precipitate from aqueous solutions at much lower concentrations than the corresponding Mg2+ salts.
Since magnesium was readily available in early evolution, it can be found in every cell type living organism. Magnesium in anaerobic prokaryotes can be found in MgATP. Magnesium also has many functions in prokaryotes such as glycolysis, all kinases, NTP reaction, signalling, DNA/RNA structures and light capture. In aerobic eukaryotes, magnesium can be found in cytoplasm and chloroplasts. The reactions in these cell compartments are glycolysis, photophosphorylation and carbon assimilation.
ATP, the main source of energy in almost all living organisms, must bind with metal ions such as Mg2+ or Ca2+ to function. Examination of cells with limited magnesium supply has shown that a lack of magnesium can cause a decrease in ATP. Magnesium in ATP hydrolysis acts as a co-factor to stabilize the high negative charge transition state. MgATP can be found in both prokaryotes and eukaryotes cells. However, most of the ATP in cells is MgATP. Following the Irving–Williams series, magnesium has a higher binding constant than the Ca2+. Therefore, the dominant ATP in living organisms is MgATP. A greater binding constant also gives magnesium the advantage as a better catalyst over other competing transition metals.
Manganese
Evidence suggests that manganese (Mn) was first incorporated into biological systems roughly 3.2–2.8 billion years ago, during the Archean Period. Together with calcium, it formed the manganese-calcium oxide complex (determined by X-ray diffraction) which consisted of a manganese cluster, essentially an inorganic cubane (cubical) structure. The incorporation of a manganese center in photosystem II was highly significant, as it allowed for photosynthetic oxygen evolution of plants. The oxygen-evolving complex (OEC) is a critical component of photosystem II contained in the thylakoid membranes of chloroplasts; it is responsible for terminal photosynthetic oxidation of water during light reactions.
The incorporation of Mn in proteins allowed the complexes the ability to reduce reactive oxygen species in Mn-superoxide dismutase (MnSOD) and catalase, in electron transfer-dependent catalysis (for instance in certain class I ribonucleotide reductases) and in the oxidation of water by photosystem II (PSII), where the production of thiobarbituric acid-reactive substances is decreased. This is due to manganese's ability to reduce superoxide anion and hydroxyl radicals as well as its chain-breaking capacity.
Iron
Iron (Fe) is the most abundant element in the Earth and the fourth most abundant element in the crust, approximately 5 percent by mass. Due to the abundance of iron and its role in biological systems, the transition and mineralogical stages of iron have played a key role in Earth surface systems. It played a larger role in the geological past in marine geochemistry, as evidenced by the deposits of Precambrian iron-rich sediments. The redox transformation of Fe(II) to Fe(III), or vice versa, is vital to a number of biological and element cycling processes. The reduction of Fe(III) is seen to oxidize sulfur (from HS to SO), which is a central process in marine sediments. Many of the first metalloproteins consisted of iron-sulphur complexes formed during photosynthesis. Iron is the main redox metal in biological systems. In proteins, it is found in a variety of sites and cofactors, including, for instance, haem groups, Fe–O–Fe sites, and iron–sulfur clusters.
The prevalence of iron is apparently due to the large availability of Fe(II) in the initial evolution of living organisms, before the rise of photosynthesis and an increase in atmospheric oxygen levels which resulted in the precipitation of iron in the environment as Fe(OH). It has flexible redox properties because such properties are sensitive to ligand coordination, including geometry. Iron can be also used in enzymes due to its Lewis acid properties, for example in nitrile hydratase. Iron is frequently found in mononuclear sites in the reduced Fe(II) form, and functions in dioxygen activation; this function is used as a major mechanism adopted by living organisms to avoid the kinetic barrier hindering the transformation of organic compounds by O. Iron can be taken up selectively as ferredoxins, Fe-O-Fe (hemerythrin and ribonucleotide reductase), Fe (many oxidases), apart from iron porphyrin. Variation in the related proteins with any one of these chemical forms of iron has produced a wide range of enzymes. All of these arrangements are modified to function both in the sense of reactivity and the positioning of the protein in the cell. Iron can have various redox and spin states, and it can be held in many stereochemistries.
Nickel and cobalt