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Chemistry of the early oceans
4 Chemistry of the early oceans: the environment of early life John Raven and Keith Skene
See Plate 2
The earliest life on Earth was in the oceans, and it is to the early ocean that we must look to find the sources of energy and chemicals used by the earliest living organisms. The energy source for early organisms is widely held to be inorganic chemical reactions, involving interactions of the ocean with the Earth's crust. An alternative view is that the energy source was from organic chemical reactions in the ocean. Since the organic chemicals would have been produced by interaction of extraterrestrial inputs (meteorites, comets, solar radiation) with atmospheric components, this view focuses on ocean/ atmosphere interactions as most significant in providing the energy for early life to the ocean. Later the direct use of light energy by organisms at the ocean surface became the major energy transforming reaction providing energy for almost all living organisms. The chemical elements which were used by the earliest organisms were determined by their availability to early organisms as well as by their physicochemical appropriateness for particular biological functions. Modification of ocean chemistry by the activities of Uving organisms, for example the acomaulation of photosynthetically produced oxygen, changed the availability of several biologically essential elements; an example is the decreased availability of iron.
Introduction Entities which have the properties of multiplication, variation and heredity can be said to be alive (MuUer, 1966; Maynard Smith and Szathmary, 1995). Such a definition of life does not specify the nature of the genetic material or of the phenotype, although it is inescapable that life always had a material basis and depended on energy dissipation. Our discussion of the chemistry of the ocean in relation to the origin and early evolution of life emphasizes how the early ocean could supply the energy and materials needed for extant life, and also of putative ancestral organisms and prebiotic components. We begin by outlining the likely chemical composition of the Hadean Ocean, including
changes to ocean chemistry due to interactions with the Earth's crust and with the atmosphere (as well as with extraterrestrial items arriving via the atmosphere). We then consider the ways in which the Hadean Ocean could have supplied the materials, and the energy, needed for the origin and early evolution of life. Finally, we briefly consider how early life could have modified the chemistry of the ocean, and how these changes could have fed back to the evolution of the early organisms.
The chemistry of the Hadean Ocean The ocean at about the time of the evolution of life, i.e. some 3.9 billion years ago (Rosing, 1999), was probably somewhat less alkaline
Evolution on Planet Earth
than the present ocean, in the sense both of p H (pH 5.5) and of mol H^-neutraHzing capacity (Holland et al., 1986; Williams and Frausto da Silva, 1996; Russell and Hall, 1997). This could perhaps be correlated with the high CO2 levels in the ocean and atmosphere (0.1-1 .OMPa; Williams and Frausto da Silva, 1996; Russell and Hall, 1997). The early ocean in equilibrium with a near-neutral (in redox terms) atmosphere was reducing, with significant Fe^"^, Mn^"^, Ni^"^ and S^~ concentrations; the low solubility of the transition metal sulfides would have limited the concentration of free sulfide in the (probable) presence of excess transition metal ions (Russell and Hall, 1997; cf. Cleaves and Miller, 1998). Russell and Hall (1997) also suggest that early seawater contained sufficient phosphate for early life. As to the bulk solutes in the early ocean, while it is widely held that the early ocean was somewhat less saline than the present ocean, there are also suggestions that the concentration of total salts was 1.5-2 times the present value (Knauth, 1998). Inputs to the early ocean came from the crust via dissolution of exposed crust, and
from hydrothermal vents, and from the atmosphere via atmospheric chemistry and extraterrestrial inputs. Inputs from exposed continental crust was not an option, since the earliest known example of such exposed continental crust comes from about 3.5 billion years ago. The inputs from hydrothermal vents would have been warmer than the bulk early ocean (i.e. above 80°C), more alkaline (up to pH 9) and more reducing (a higher concentration of S^-): Williams and Frausto da Silva (1996); Russell and Hall (1997). This fluid would also contain NH3 produced by reduction of N2 using metallic iron or reduced iron oxides in localized low H20-regions in the lithosphere at high temperature (300-800°C) and pressure (100 MPa), providing perhaps 1-100 Gmol NH3 per year (Table 4.1). The early atmosphere could have produced NO* by reactions of N2 with H2O and CO2 energized by lightning or meteorite passage. Dissolution of these NO -free radicals would produce NOJ and NO^, which could be reduced to NH3 in the ocean using Fe compounds (see Raven and Yin, 1998; Brandes et
evehitfofi ^ Mtf mA H Rav«ti msA ISm <199S^ Md Flux
Magnitude
Atmospheric N2 conversion to NO* by oxidization with CO2 or H2O energized by lightning or meteorite impacts; dissolution of NO' and formation of N02~; reduction of N02~ to NH4"^ (in the early ocean)
< 50 Gmol NH4^ per year
Catalysis of NH4^ production by Ti (on early Earth and today)
< 4 Gmol NH4"^ per year
N2 reduction to NH3 by metallic Fe or reduced iron oxides in localized I0W-H2O, high temperature (300-^00°C) and pressure (100 MPa), followed by efflux as NH4^ to the ocean in hydrothermal vents (on early Earth and today)
1-100 Gmol NH4+ per year
Biological N2 fixation in extant ocean
~ 1 Tmol NH4'^ per year
Global assimilation of combined N (mainly NH4"^, NO3") by primary producers in the extant ocean
~ 420 mol N per year
Global NO;c production by lightning in present atmosphere (over ocean and land) today
~ 1 Tmol NO^ * per year
Chemistry of the early oceans: the environment of early life
al., 1998) at rates similar to these suggested (above) for NH3 input from hydrothermal vents (Table 4.1). Brandes et al. (1998) suggested that the oceanic NH3 could produce an atmospheric NH3 partial pressure adequate to permit a sufficient NH3 greenhouse effect. This would have significantly offset the 'weak young Sun' and hence help maintain liquid water on the Earth's surface, provided that UV-induced breakdown of atmospheric NH3 is restricted by high altitude UV-absorbing organic haze (Brandes et al, 1998; Chyba, 1998). As for abiogenic production of organic-C, there is no obvious way in which organic-C could be produced in the bulk ocean. Production of organic-C would have involved interactions with the lithosphere and the atmosphere. Organic-C production in the early ocean in association with the lithosphere could have involved interaction of the early ocean with the iron sulphur minerals at the lithosphere/hydrosphere interface (Wachterhauser, 1990), a n d / o r the interaction of the alkaline, strongly reducing hydrothermal vent solution with the less alkaline, less reducing bulk seawater, possibly via an iron monosulfide membrane which forms spontaneously at the vent fluid/bulk seawater interface (Russell and Hall, 1997) (Table 4.2). The possibility of an atmospheric involvement seems less likely now, with the widespread assumption of a neutral atmosphere (predominantly CO2/N2/H2O), than at the time of the
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Urey-Miller experiments (early 1950s) which were predicated on a reducing Hadean atmosphere (Broecker, 1985; Maynard Smith and Szathmary, 1995). Thus, the production of significant quantities of protein amino acids and nucleic acid bases were produced from energization of a reducing atmosphere (H2, CH4, NH3, H2O) by an electric discharge mimicking the electrical discharge of a thunderstorm in the early atmosphere. However, when this experiment is repeated with a neutral (CO2/ N2/H2O) atmosphere, very little organic material, such as amino acids and nucleic acid bases, is produced. Possible additional sources of organic sources from above the ocean include the suggestion of Woese (1979) of chemical evolution in water droplets in clouds, and the suggestion of Oro (1961) of organic carbon delivery by comets and meteorites. The suggestion of water droplets as an important seat of organic compound production can, to the extent that the water droplets could have entrained mineral particles, be considered an extension of the hydrosphere/lithosphere interface (Maynard Smith and Szathmary, 1995; cf. Cairns-Smith and Hartman, 1986; Wachterhauser, 1990). Delivery of organic matter by impacting comets and meteorites (Oro, 1961) requires a relatively high total atmospheric pressure (1 MPa at the Earth's surface, mainly as CO2) to limit destruction of organic matter en route to the surface (Maynard Smith and
Flux
Magnitude
Chemolithotrophic inorganic-C reduction using reductant from hydrothermal vents on the early Earth (and today)
< 50 Gmol C per year
Photolithotrophic inorganic-C reduction in the extant ocean
- 5 Fmol C per year
Chemolithotrophic inorganic-C reduction related to nitrification of NH4^ to N02~ and of N02~ to NOa" in the extant ocean (NH4'^ comes mainly from viral lysis, grazing phytoplankton followed by excretion of NH4"^; O2 comes from photosynthesis)
-16 Tmol C per year
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Evolution on Planet Earth
Szathmary, 1995). With ten times the present atmospheric density organic carbon from comets might reach the Earth at a rate of as much as 0.1-1 .OGmol C of organic matter per year (Chyba et al, 1990) (cf. Table 4.2).
How could the early ocean supply material for the origin and early evolution of life? Here we look at the chemistry of the early ocean (as discussed above) in the context of the need for elements (and their chemical forms) for life. The perceptive reader may have detected a bias in the direction of the elements known to be used in present-day life in that discussion of early ocean chemistry. At all events, the elements used in organisms must not only have the appropriate chemical properties, but also have been available at the time of the origin and early evolution of life (Williams and Frausta da Silva, 1996). The listing of essential elements given below is based on Marschner (1995) and Williams and Frausta da Silva (1996); see also Raven and Smith (1981). H: Essential for all organisms; obtained from H2O B: Essential for some organisms; obtained from B(OH)3 C: Essential for all organisms; obtained from inorganic C (C02/HC03"/C03^") and any organic C produced prebiotically N: Essential for all organisms; obtained from NH3/NH4' produced prebiotically as described earlier. Biota subsequently evolved the capacity to use N2 and NO3 (via their conversion to N H 3 / N H I ) O: Essential for all organisms; obtained from H2O, inorganic C and (much later, and to a limited extent) O2 Na: Essential for some organisms; obtained from Na"^ in seawater Mg: Essential for all organisms; obtained from Mg^"^ in seawater
Si: Essential for some organisms; obtained from Si(OH4) in seawater P: Essential for all organisms; obtained from HP04^~ in seawater S: Essential for all organisms; obtained from S^~ in seawater and, much later, from S04^~, derived mainly via oxidation of S^~ by (inter alia) O2 CI: Essential for some organisms; obtained from Cl~ in seawater K: Essential for all organisms; obtained from K"^ in seawater Ca: Essential for all organisms; obtained from Ca^"^ in seawater Mn: Essential for all organisms; obtained from Mn^"^ in seawater Fe: Essential for all organisms; obtained from Fe^"^ in seawater and, much later from Fe^"^ in seawater following oxidation by (inter alia) O2 Co: Essential for many organisms; obtained from Co^"^ in seawater Ni: Essential for most organisms; obtained from Ni^"^ in seawater Cu: Essential for all organisms; very scarce in early ocean (CU2S very insoluble), later available as Cu^"^ in seawater Zn: Essential for all organisms; obtained from Zn^"^ in seawater Se: Essential for most organisms; obtained from Se^~ in seawater, later available as Se03^~ and Se04^~ in seawater Mo: Essential for all organisms; obtained from Mo04^~ in seawater I: Essential for some organisms; obtained as I~, IO3" in seawater The elements listed above are required over a very wide range of concentrations in biota, where 'required' is defined by the concentration in biomass which permits the organism to achieve its maximum metabolic and growth potential. In terms of number of atoms, H and O dominate through the occurrence of H2O as more than half of the biomass of essentially all organisms. On the basis of H20-free biomass H, C and O dominate, with N, P, K, S, Mg and Ca comprising the other 'major' essential elements. The other essential elements are needed in much smaller amounts (10~^-10"^ that of C).
Chemistry of the early oceans: the environment of early life
How could the early ocean supply energy for the origin and early evolution of life? Life requires a continual input of free energy for the growth and maintenance of organisms. The free energy transformed by organisms can, in principle, come from a very wide range of sources, for example mechanical energy (e.g. water flow over an attached organism) and osmotic potential energy (e.g. tidal changes in external salinity in an estuary). In the absence of significant evidence for such energy sources in extant organisms, we deal here with catalysis of the coupling of energy from light, or organic chemical, or inorganic chemical reactions, to essential processes in the origin of life, and the early evolution of life. In all cases energy is dissipated during the energy transformations; less energy is stored in the products than was present in the substrate if a net conversion of useful energy is to take place. In addition to coupling the exergonic reaction to the (pre)biologically significant endergonic reaction, catalysis is involved in speeding the exergonic reaction which is based on energetic disequilibrium. Dealing first with photochemistry, solar radiation is not, of course, endogenous to the sea. There is a very weak radiation, some of which is at wavelengths which could be involved in profitable photochemistry, in the ocean as a result at least in part of sonoluminescence involving thermal excitation of Na"^ ions (Matula, 1999; Hilgenfeldt et ah, 1999). However, it is not certain that the radiation is quantitatively sufficient to support photosynthetic life (see Yurkov and Beatty, 1998). Furthermore, it is likely that at least some of this radiation comes today from the spontaneous oxidation of sulfide by molecular oxygen (Tapley et al., 1999). This mechanism would not have been available to the earliest life forms with ready access to sulfide, especially at hydrothermal vents, but with negligible molecular oxygen available until biological production of this gas evolved. One of the inorganic sinks for this oxygen which delayed its accumulation in the biosphere was, of course, this photon-emitting oxidation of sulfide.
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Solar radiation is clearly adequate to support photosynthesis amounting globally to some 4Pmol inorganic-C converted to organic-C each year in the present ocean (Falkowski and Raven, 1997; Table 4.2). However, this productivity is confined to the upper 300 m of even the most transparent seawater as a result of the photon absorption properties of H2O. Generally there are other absorbing and scattering materials in seawater which attenuate solar radiation and decrease the depth at which photosynthetic growth can occur. All natural waters, regardless of their O2 content, attenuate UV radiation more than photosynthetically active radiation (Kirk, 1994a, b). While photochemical energization of the earliest living cells is neither likely nor widely advocated, it is possible that photochemistry in the ocean, and especially in the atmosphere, was important in generating particular chemical species related to the origin of life. Turning to the energization of early life by organic chemical reactions (chemo-organotrophy), this requires a prebiotic generation of organic matter. This could result from atmospheric (energized by UV radiation, lightning or meteorite impacts), crustal (including hydrothermal vent/bulk seawater interactions, and reactions at the crust/seawater interface) or extraterrestrial (coming to Earth on comets) events. It also requires that some reaction of the organic substrate is exergonic, by an internal rearrangement of the organic substrate, including its dismutation, or by reaction with some other organic or inorganic molecule (see Broda, 1975). Current views are that this is not the most likely means of energizing the earliest cells (see Edwards, 1998). The third possibility is that the earliest cells were chemolithotrophic, i.e. were energized by inorganic chemical reactions. This currently popular hypothesis is supported by molecular phylogenetic evidence suggesting that the root of the universal tree of life is in extant chemolithotrophic (and thermophilic) organisms (Pace, 1997). Suggestions have been made of chemically (Wachterhauser, 1990) and geologically (Russell and Hall, 1997, 1999) explicit models of a chemolithotrophic energization of
60
Evolution
on Planet Earth
the origin of life and of the earhest organisms (Table 4.2). The chemically explicit models of Wachterhauser (1990) relate to surface chemistry in the Hadean Ocean which can drive reactions such as FeS + H2S + CO2 -^ FeS2 +HCC)OH, and subsequently the reactions of the reverse tricarboxylic acid cycle. Russell and Hall (1997, 1999) base their mechanism of energy transduction on the hotter, more reducing, more alkaline solution emanating from hydrothermal vents reacting with the warm, less reducing, less alkaline bulk seawater. The reaction is suggested to occur across an iron monosulfide layer which forms spontaneously between the two solu-
4.3 Billion years ago ^^•••'••'•^r^i.,,,.^.^^
tions. Russell and Hall (1997, 1999) suggest that this 'membrane' could act as the place in which exergonic redox reactions (more reducing inner phase, less reducing outer phase) and H"^ fluxes (from the less alkaline outer phase to the more alkaline inner phase) could energize essential biosyntheses. How this occurred, and how the iron monosulfide 'membrane' became a lipoprotein biological membrane, needs further clarification (see Blobel, 1980; Koch and Schmidt, 1991; Edwards, 1998; Russell and Hall, 1999). The Russell and Hall (1997, 1999) scheme for a chemolithotrophic origin of life is shown in Figure 4.1 in the context of Mars 4.3 billion years ago (Early Noachian). Atmosphere <10 bars of CO2 with CO, SO2 and N2 but very low O2
mmEmocEAM Hot-sprtr^
Volcanic oceanic crust (mafic/ultramafic)
5 km
Descending 1 ocean water
Alkaline hydrothermal solution 200°C PH
Oxidation Hydration .Carbonation -250°C
COp
1 mm
Figure 4.1 Model environment for the emergence of life on Earth or Mars (reproduced with permission from Russell, M.J. and Hall, Allen J. (1997/1999) On the inevitable emergence of life in Mars (Julian A. Muscot, ed.). The Search for Life on Mars. Proceedings of the 1st UK Conference, British Interplanetary Society, London) by chemolithotrophic mechanism, related specifically to the putative Early Noachian (Mars 4.3 billion years ago) ocean floor at a submarine alkaline hot spring. The mechanism proposes that the fatty acids which compose the organic membrane which replaced the iron monosulfide were generated in the iron monosulfide compartments comprising the sulfide mound.
Chemistry of the early oceans: the environment of early life This model of the energization of the early iron monosulfide 'membrane' and the early lipoprotein membranes in terms of an electrochemical potential gradient of H"^, involving chemiosmotic reactions (Koch and Schmidt, 1991; cf. Raven and Smith, 1981, 1982), is based on an early ocean which was acidic or near-neutral (Kasting, 1993; Russell and Hall, 1997, 1999). It is important to realize that there are alternatives to this notion of an acidic early ocean, e.g. the early soda ocean suggestions of Kempe and Degens (1985) and Kempe and Kazmierczak (1997). The suggestions as to the evolution of H"^ active transport across membranes and of chemiosmotic reactions of Raven and Smith (1981, 1982) were in fact based on a neutral or slightly alkaline early ocean, albeit not in the context of a chemolithotrophic origin of life and chemolithotrophic energization of the earliest cells. The lack of calcification of the earliest organisms accords better with an acidic rather than an alkaline early ocean. An acidic early ocean would, in equilibrium with more than 0.1 MPa partial pressure of CO2, have both a high concentration of CO2 (in excess of 40molm~^ CO2). There would also be a high concentration of HCOs", at least 4molm"^ with a pH of 5, i.e. at least twice the concentration in today's sea water with a pH of 8.0 in equilibrium with 33 Pa CO2 in the atmosphere. This high CO2 concentration in the early ocean (regardless of its pH, providing it is in equilibrium with at least 0.1 Ma CO2 in the atmosphere) would be adequate to saturate the carboxylase enzyme(s) of any known autotrophic or anaplerotic inorganic carbon fixation (Raven, 1991, 1997a, b, c). This conclusion is independent of whether the enzymes use CO2 or HCOs" as their immediate substrate (provided that the intracellular pH is maintained close to neutrality), or of whether there is a significant diffusion restriction of CO2 entry (Raven, 1991, 1997a, b, c). At all events, CO2 diffusion through water and the lipid component of lipoprotein bilayers would have been adequate to supply inorganic carbon to the carboxylases; no inorganic carbon concentrating mechanisms would have been needed.
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Although much needs to be clarified, the chemolithotrophic energization of the earliest biota seems to be the best currently available hypothesis.
How did early biota cliange ocean cliemistry and how did these chemical changes influence the early evolution of life? We assume a chemolithotrophic origin of life, and chemolithotrophy as the earliest energetic coupling mechanism in biota. In quantitative terms it is likely that the rate of reductant input from hydrothermal vents would limit worldwide primary production each year to about SOGmole, at least inasmuch as input through vents is concerned (Jakosky and Shock, 1998). A parallel input of chemolithotrophic substrates could come from the sorts of reactions discussed by Wachterhauser (1990). However, quantifying the productivity based on such energization is more complex, and will not be attempted here. To this 'new' productivity could be added 'recycled' productivity, which could result from the regeneration of inorganic reductant and inorganic carbon from 'respiratory' metabolism of the organic carbon and inorganic oxidant generated in chemolithotrophy. Such cycles of recycled chemolithotrophic productivity and 'respirationbased' productivity would run down, for example by sedimentation of reactants such as organic carbon (and inorganic oxidant?). Thus there is likely to have been an incomplete recycling of the products of chemolithotrophy to regenerate reductant at a sufficient reducing redox potential to reduce inorganic carbon to sugars. However, additional productivity could result from an additional energy input which could generate a strong reductant from a weaker reductant. Such an energy input could come from photons in the process of photosynthesis, permitting growth by photolithotrophy. However, thus far we have been implicitly considering biota at great depth in the ocean, centred on hydrothermal vents. These biota would have not suffered from
62
Evolution on Planet Earth
damage from the higher than present UV output from the young Sun, unscreened by the atmosphere due to the absence of O2, and hence UV-absorbing O3, in the atmosphere, due to the great depth of UV-absorbing water (Kirk, 1994a). However, despite the lower attenuation of photosynthetically active radiation than of damaging (UV-B) UV radiation by natural seawaters as has been mentioned earlier, no photosynthetically significant radiation from the Sun penetrates to 300 m even in the clearest waters. As to why the biota should occur close enough to the ocean surface to permit photosynthesis, we can suggest that chemolithotrophs were exploiting inorganic reductants in near-surface sediments. A plausible model for the evolution of photosynthesis from UV-screening protein-pigment systems is given by Mulkidjanian and Junge (1997). Here the UV was screened out by absorption of UV by membrane-associated proteins, with associated pigments (cyclic tetrapyrrols) able to accept excitation energy transferred from the protein, with energy dissipation by fluorescence, heat or photochemistry. The photochemical option for dissipation of UV energy could generate a strong reductant from a weaker reductant. Eventually, the energization of this process came to rely almost entirely on the absorption directly by the tetrapyrrol pigments of longer wavelength (>400 nm) radiation. In such organisms the UV-screening protein-pigment complexes evolved independently into two kinds of reaction centers of the RCl and the RC2 types (Mulkidjanian and Junge, 1997). Both of these can bring about inorganic carbon reduction to sugars using reductant originally derived from weak reductants such as S^~. Ultimately even weak reductants such as Fe and S;'/-~ would be locally exhausted, as sedimentation of the organic product of primary production prevented the respiratory regeneration of Fe^"^ from Fe^"^ and S from S° and S04^~. Such local depletion of weak reductants means that continued photosynthetic generation of strong reductants which could reduce inorganic carbon to carbohydrates, required the substitution of an even
weaker reductant for the S^~ and Fe^"^. This even weaker reductant is H2O which is, for all biotic purposes, infinitely available in sea water. The energy required to move an electron from H2O to a reductant strong enough to reduce inorganic carbon to produce sugars is significantly greater than that needed for the use of a stronger reductant as electron donor. Accordingly all 02-evolving organisms (i.e. those using H2O as their electron donor) have both an RCl and an RC2 reaction involved in transferring an electron from H2O to CO2, so that the energy from two photons (one used in the RCl, the other in the RC2) is used to transfer the 'electron'. In evolutionary terms what is needed here is a horizontal gene transfer so that RCl and RC2 can be expressed in a single cell. Furthermore, the redox span covered by RC2 is shifted toward more oxidizing potentials, so that the oxidant generated by this RC2 can oxidize H2O to produce O2, but the reductant generated by this RC2 is certainly incapable of reducing inorganic carbon to sugars (Olson and Pierson, 1986; Trissl and Wilhelm, 1993). The remainder of the redox span to the redox level needed to reduce inorganic carbon to carbohydrates is covered by RCl. The ability to use H2O as the ultimate electron donor for inorganic carbon fixation, with consequent O2 production, increases the ability of photosynthetic organisms to oxidize the S^~ and Fe^"^ in the ocean over and above the direct oxidation of S^" and Fe^"^ by organisms with RCl or RC2. O2 build-up in the atmosphere requires that the O2 produced in photosynthesis is not entirely consumed in respiration of the other product of photosynthesis, i.e. organic carbon sedimentation and long-term storage of this organic carbon is needed. O2 accumulation in the atmosphere also requires that the S^~ and Fe^"^ sinks for O2 have been oxidized; these S^~ and Fe^"^ sinks are not just the pre-existing pools in the ocean, but also the continued input from hydrothermal vents. Finally, the presence of O2 in the atmosphere permits oxidation of Fe^"^ and S^~ exposed on the continental crust, first found some 3.5 billion years ago (Buick et al., 1995; Raven, 1997a), again forming a sink for O2 which must be satisfied before O2 can further increase in the atmosphere.
Chemistry of the early oceans: the environment of early life The build-up of O2 would diminish the availability of Fe and Mn to 02-evolving photosynthetic organisms due to the insolubility of the Fe203 and Mn02 which form under oxidizing conditions. However, Cu becomes much more available under these conditions, as the soluble Cu^"^ instead of the very insoluble CU2S. The implications of this for the functioning, and subsequent evolution, of photosynthetic 02-evolvers is discussed by Raven et al. (1999). Furthermore, organic matter can scavenge Mo from seawater, thus providing another feedback of the evolution of life on the chemistry of the oceans, in this case with implications for the capacity of organisms to acquire N for N2 and NO^ via Mo-requiring nitrogenase and nitrate reductase enzymes (Holland et al, 1986; Falkowski, 1997; Falkowski and Raven, 1997).
Conclusion The early ocean provided all of the elemental requirements for the origin and early evolution of life, although some inputs from the atmosphere and crust were needed to provide the appropriate chemical species. The chemistry of life is determined by both the appropriate chemical properties of a given element and its availability. Some essential elements (e.g. P) may not have been abundant at any stage during the origin and early evolution of life. Inorganic chemical reactions are the only energy sources for the origin of life which are endogenous to the early ocean, especially if the crust/ocean interface is acceptable as part of the ocean. These inorganic chemical energy sources (e.g. involving Fe and S) could allow a chemolithotrophic energization of the origin and early evolution of life. Additional energy inputs could come from the more alkaline and reducing solution from hydrothermal vents which is out of energetic equilibrium with the less alkaline, less reducing, seawater. Early life modified the chemistry of the early ocean. In conjunction with the sedimentation of organic reduced products of chemolithotrophs (and possibly of the oxidized inorganic pro-
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duct), chemolithotrophy would decrease the availability of inorganic reductant for chemolithotrophy. This modification to the medium, together with use of some of the metabolic machinery involved in chemolithotrophy, provides both selection pressure and some part of the mechanism for the evolution of photolithotrophy.
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Jakosky, B.M. and Shock, E.L. (1998). The biological potential of Mars, the early Earth and Europa. Journal of Geophysical Research, 103: 19359-19364. Kasting, J.F. (1993). Earth's early atmosphere. Science, 259: 920-926. Kempe, S. and Degens, E.T. (1985). An early soda ocean? Chemical Geology, 53: 95-108. Kempe, S. and Kazmierczak J. (1997). A terrestrial model for an alkaline Martian atmosphere. Planetary and Space Science, 45: 1493-1499. Kirk, J.T.O. (1994a). Optics of UV-radiation in natural water. Archiv fur Hydrobiologie Beihefte, 43: 1-16. Kirk, J.T.O. (1994b). Light and Photosynthesis in Aquatic Systems. Second Edition. Cambridge: Cambridge University Press. Knauth, L.P. (1998). Salinity history of the Earth's early ocean. Nature, 395: 554r-555. Koch, A.L. and Schmidt, T.M. (1991). The 1st cellular bioenergetic process - primitive generation of a proton-motive force, journal of Molecular Evolution, 33: 297-304. Marschner, H. (1995). Mineral Nutrition of Higher Plants. Second Edition. London: Academic Press. Matula, T.J. (1999). Inertial cavitation and singlebubble sonoluminescence. Philosophical Transactions of the Royal Society of London A, 357: 225-249. Maynard Smith, J. and Szathmary, E. (1995). The Major Transitions in Evolution. Oxford: Oxford University Press. Mulkidjanian, A.Y. and Junge, W. (1997). On the origin of photosynthesis as inferred from sequence analysis a primordial UV-protection as common ancestor of reaction center and antenna proteins. Photosynthesis Research, 51: 27-42. MuUer, H.J. (1966). The gene material as the initiator and organizing basis of life. American Naturalist, 100: 493-517. Olson, J.M. and Pierson, B.K. (1986). Photosynthesis 3.5 thousand million years ago. Photosynthesis Research, 9: 251-259. Oro, J. (1961). Comets and the formation of biochemical compounds on the primitive Earth. Nature, 190: 389. Pace, N.R. (1997). A molecular view of microbial diversity and the biosphere. Science, T7^\ 734-740. Raven, J.A. (1991). ImpUcations of inorganic C utilization: ecology, evolution and geochemistry. Canadian journal of Botany, 69: 908-924. Raven, J.A. (1996). The role of autotrophs in global CO2 cycling. In: M.E. Lidstrom and F.R. Tabita (eds) Microbial Growth on Ci Compounds. Dordrecht: Kluwer Academic Publishers, pp. 351-358.
Raven, J.A. (1997a). The role of marine biota in the evolution of terrestrial biota: gases and genes. Biogeochemistry, 39: 139-164. Raven, J.A. (1997b). Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research, 27: 85-209. Raven, J.A. (1997c). Putting the C in phycology. European journal of Phycology, 32: 319-333. Raven, J.A. and Smith, F.A. (1981). H^" transport and the evolution of photosynthesis. Biosystems, 14: 95-111. Raven, J.A. and Smith, F.A. (1982). Solute transport at the plasmalemma and the early evolution of cells. Biosystems, 15: 13-26. Raven, J.A. and Yin, Z.-H. (1998). The past, present and future of nitrogenous compounds in the atmosphere and their interactions with plants. New Phytologist, 139: 205-219. Raven, J.A., Evans, M.C.W. and Korb, R.E. (1999). The role of trace metals in photosynthetic electron transport in 02-evolving organisms. Photosynthesis Research, 60: 111-149. Rosing, M.T. (1999). ^^C-depleted carbon microparticles in >3700Ma sea-floor sedimentary rock from West Greenland. Science, 283: 674-676. Russell, M.J. and Hall, A.J. (1997). The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front, journal of the Geological Society, London, 154: 377-402. Russell, M.J. and Hall, A.J. (1999). On the inevitable emergence of life on Mars. British Interplanetary Society Proceedings, 26-36. ISSN 0007-09-4X. Tapley, D.W., Buettner, G.R. and Shick, J.M. (1999). Free radicals and chemiluminescence as products of the spontaneous oxidation of sulfide in seawater, and their biological implications. Biological Bulletin, 196: 52-56. Trissl, H.-W. and Wilhelm, C. (1993). Why do thylakoid membranes from higher plants form grana stacks? Trends in Biochemical Science, 18: 415^18. Wachterhauser, G. (1990). Evolution of the first metabolic cycles. Proceedings of the National Academy of Sciences, 87: 200-204. Williams, R.J.P. and Frausto da Silva, J.J.R. (1996). The Natural Selection of the Chemical Elements. The Environment and Life's Chemistry. Oxford: Clarendon Press. Woese, C.R. (1979). A proposal concerning the origin of life on Earth, journal of Molecular Evolution, 13: 95-101. Yurkov, V. and Beatty, J.T. (1998). Isolation of aerobic anoxygenic photosynthetic bacteria from black smoker plume waters off the Juan de Fuca ridge in the Pacific Ocean. Applied and Environmental Microbiology, 64: 337-349.
See Plate 2
The earliest life on Earth was in the oceans, and it is to the early ocean that we must look to find the sources of energy and chemicals used by the earliest living organisms. The energy source for early organisms is widely held to be inorganic chemical reactions, involving interactions of the ocean with the Earth's crust. An alternative view is that the energy source was from organic chemical reactions in the ocean. Since the organic chemicals would have been produced by interaction of extraterrestrial inputs (meteorites, comets, solar radiation) with atmospheric components, this view focuses on ocean/ atmosphere interactions as most significant in providing the energy for early life to the ocean. Later the direct use of light energy by organisms at the ocean surface became the major energy transforming reaction providing energy for almost all living organisms. The chemical elements which were used by the earliest organisms were determined by their availability to early organisms as well as by their physicochemical appropriateness for particular biological functions. Modification of ocean chemistry by the activities of Uving organisms, for example the acomaulation of photosynthetically produced oxygen, changed the availability of several biologically essential elements; an example is the decreased availability of iron.
Introduction Entities which have the properties of multiplication, variation and heredity can be said to be alive (MuUer, 1966; Maynard Smith and Szathmary, 1995). Such a definition of life does not specify the nature of the genetic material or of the phenotype, although it is inescapable that life always had a material basis and depended on energy dissipation. Our discussion of the chemistry of the ocean in relation to the origin and early evolution of life emphasizes how the early ocean could supply the energy and materials needed for extant life, and also of putative ancestral organisms and prebiotic components. We begin by outlining the likely chemical composition of the Hadean Ocean, including
changes to ocean chemistry due to interactions with the Earth's crust and with the atmosphere (as well as with extraterrestrial items arriving via the atmosphere). We then consider the ways in which the Hadean Ocean could have supplied the materials, and the energy, needed for the origin and early evolution of life. Finally, we briefly consider how early life could have modified the chemistry of the ocean, and how these changes could have fed back to the evolution of the early organisms.
The chemistry of the Hadean Ocean The ocean at about the time of the evolution of life, i.e. some 3.9 billion years ago (Rosing, 1999), was probably somewhat less alkaline
Evolution on Planet Earth
than the present ocean, in the sense both of p H (pH 5.5) and of mol H^-neutraHzing capacity (Holland et al., 1986; Williams and Frausto da Silva, 1996; Russell and Hall, 1997). This could perhaps be correlated with the high CO2 levels in the ocean and atmosphere (0.1-1 .OMPa; Williams and Frausto da Silva, 1996; Russell and Hall, 1997). The early ocean in equilibrium with a near-neutral (in redox terms) atmosphere was reducing, with significant Fe^"^, Mn^"^, Ni^"^ and S^~ concentrations; the low solubility of the transition metal sulfides would have limited the concentration of free sulfide in the (probable) presence of excess transition metal ions (Russell and Hall, 1997; cf. Cleaves and Miller, 1998). Russell and Hall (1997) also suggest that early seawater contained sufficient phosphate for early life. As to the bulk solutes in the early ocean, while it is widely held that the early ocean was somewhat less saline than the present ocean, there are also suggestions that the concentration of total salts was 1.5-2 times the present value (Knauth, 1998). Inputs to the early ocean came from the crust via dissolution of exposed crust, and
from hydrothermal vents, and from the atmosphere via atmospheric chemistry and extraterrestrial inputs. Inputs from exposed continental crust was not an option, since the earliest known example of such exposed continental crust comes from about 3.5 billion years ago. The inputs from hydrothermal vents would have been warmer than the bulk early ocean (i.e. above 80°C), more alkaline (up to pH 9) and more reducing (a higher concentration of S^-): Williams and Frausto da Silva (1996); Russell and Hall (1997). This fluid would also contain NH3 produced by reduction of N2 using metallic iron or reduced iron oxides in localized low H20-regions in the lithosphere at high temperature (300-800°C) and pressure (100 MPa), providing perhaps 1-100 Gmol NH3 per year (Table 4.1). The early atmosphere could have produced NO* by reactions of N2 with H2O and CO2 energized by lightning or meteorite passage. Dissolution of these NO -free radicals would produce NOJ and NO^, which could be reduced to NH3 in the ocean using Fe compounds (see Raven and Yin, 1998; Brandes et
evehitfofi ^ Mtf mA H Rav«ti msA ISm <199S^ Md Flux
Magnitude
Atmospheric N2 conversion to NO* by oxidization with CO2 or H2O energized by lightning or meteorite impacts; dissolution of NO' and formation of N02~; reduction of N02~ to NH4"^ (in the early ocean)
< 50 Gmol NH4^ per year
Catalysis of NH4^ production by Ti (on early Earth and today)
< 4 Gmol NH4"^ per year
N2 reduction to NH3 by metallic Fe or reduced iron oxides in localized I0W-H2O, high temperature (300-^00°C) and pressure (100 MPa), followed by efflux as NH4^ to the ocean in hydrothermal vents (on early Earth and today)
1-100 Gmol NH4+ per year
Biological N2 fixation in extant ocean
~ 1 Tmol NH4'^ per year
Global assimilation of combined N (mainly NH4"^, NO3") by primary producers in the extant ocean
~ 420 mol N per year
Global NO;c production by lightning in present atmosphere (over ocean and land) today
~ 1 Tmol NO^ * per year
Chemistry of the early oceans: the environment of early life
al., 1998) at rates similar to these suggested (above) for NH3 input from hydrothermal vents (Table 4.1). Brandes et al. (1998) suggested that the oceanic NH3 could produce an atmospheric NH3 partial pressure adequate to permit a sufficient NH3 greenhouse effect. This would have significantly offset the 'weak young Sun' and hence help maintain liquid water on the Earth's surface, provided that UV-induced breakdown of atmospheric NH3 is restricted by high altitude UV-absorbing organic haze (Brandes et al, 1998; Chyba, 1998). As for abiogenic production of organic-C, there is no obvious way in which organic-C could be produced in the bulk ocean. Production of organic-C would have involved interactions with the lithosphere and the atmosphere. Organic-C production in the early ocean in association with the lithosphere could have involved interaction of the early ocean with the iron sulphur minerals at the lithosphere/hydrosphere interface (Wachterhauser, 1990), a n d / o r the interaction of the alkaline, strongly reducing hydrothermal vent solution with the less alkaline, less reducing bulk seawater, possibly via an iron monosulfide membrane which forms spontaneously at the vent fluid/bulk seawater interface (Russell and Hall, 1997) (Table 4.2). The possibility of an atmospheric involvement seems less likely now, with the widespread assumption of a neutral atmosphere (predominantly CO2/N2/H2O), than at the time of the
57
Urey-Miller experiments (early 1950s) which were predicated on a reducing Hadean atmosphere (Broecker, 1985; Maynard Smith and Szathmary, 1995). Thus, the production of significant quantities of protein amino acids and nucleic acid bases were produced from energization of a reducing atmosphere (H2, CH4, NH3, H2O) by an electric discharge mimicking the electrical discharge of a thunderstorm in the early atmosphere. However, when this experiment is repeated with a neutral (CO2/ N2/H2O) atmosphere, very little organic material, such as amino acids and nucleic acid bases, is produced. Possible additional sources of organic sources from above the ocean include the suggestion of Woese (1979) of chemical evolution in water droplets in clouds, and the suggestion of Oro (1961) of organic carbon delivery by comets and meteorites. The suggestion of water droplets as an important seat of organic compound production can, to the extent that the water droplets could have entrained mineral particles, be considered an extension of the hydrosphere/lithosphere interface (Maynard Smith and Szathmary, 1995; cf. Cairns-Smith and Hartman, 1986; Wachterhauser, 1990). Delivery of organic matter by impacting comets and meteorites (Oro, 1961) requires a relatively high total atmospheric pressure (1 MPa at the Earth's surface, mainly as CO2) to limit destruction of organic matter en route to the surface (Maynard Smith and
Flux
Magnitude
Chemolithotrophic inorganic-C reduction using reductant from hydrothermal vents on the early Earth (and today)
< 50 Gmol C per year
Photolithotrophic inorganic-C reduction in the extant ocean
- 5 Fmol C per year
Chemolithotrophic inorganic-C reduction related to nitrification of NH4^ to N02~ and of N02~ to NOa" in the extant ocean (NH4'^ comes mainly from viral lysis, grazing phytoplankton followed by excretion of NH4"^; O2 comes from photosynthesis)
-16 Tmol C per year
;8
Evolution on Planet Earth
Szathmary, 1995). With ten times the present atmospheric density organic carbon from comets might reach the Earth at a rate of as much as 0.1-1 .OGmol C of organic matter per year (Chyba et al, 1990) (cf. Table 4.2).
How could the early ocean supply material for the origin and early evolution of life? Here we look at the chemistry of the early ocean (as discussed above) in the context of the need for elements (and their chemical forms) for life. The perceptive reader may have detected a bias in the direction of the elements known to be used in present-day life in that discussion of early ocean chemistry. At all events, the elements used in organisms must not only have the appropriate chemical properties, but also have been available at the time of the origin and early evolution of life (Williams and Frausta da Silva, 1996). The listing of essential elements given below is based on Marschner (1995) and Williams and Frausta da Silva (1996); see also Raven and Smith (1981). H: Essential for all organisms; obtained from H2O B: Essential for some organisms; obtained from B(OH)3 C: Essential for all organisms; obtained from inorganic C (C02/HC03"/C03^") and any organic C produced prebiotically N: Essential for all organisms; obtained from NH3/NH4' produced prebiotically as described earlier. Biota subsequently evolved the capacity to use N2 and NO3 (via their conversion to N H 3 / N H I ) O: Essential for all organisms; obtained from H2O, inorganic C and (much later, and to a limited extent) O2 Na: Essential for some organisms; obtained from Na"^ in seawater Mg: Essential for all organisms; obtained from Mg^"^ in seawater
Si: Essential for some organisms; obtained from Si(OH4) in seawater P: Essential for all organisms; obtained from HP04^~ in seawater S: Essential for all organisms; obtained from S^~ in seawater and, much later, from S04^~, derived mainly via oxidation of S^~ by (inter alia) O2 CI: Essential for some organisms; obtained from Cl~ in seawater K: Essential for all organisms; obtained from K"^ in seawater Ca: Essential for all organisms; obtained from Ca^"^ in seawater Mn: Essential for all organisms; obtained from Mn^"^ in seawater Fe: Essential for all organisms; obtained from Fe^"^ in seawater and, much later from Fe^"^ in seawater following oxidation by (inter alia) O2 Co: Essential for many organisms; obtained from Co^"^ in seawater Ni: Essential for most organisms; obtained from Ni^"^ in seawater Cu: Essential for all organisms; very scarce in early ocean (CU2S very insoluble), later available as Cu^"^ in seawater Zn: Essential for all organisms; obtained from Zn^"^ in seawater Se: Essential for most organisms; obtained from Se^~ in seawater, later available as Se03^~ and Se04^~ in seawater Mo: Essential for all organisms; obtained from Mo04^~ in seawater I: Essential for some organisms; obtained as I~, IO3" in seawater The elements listed above are required over a very wide range of concentrations in biota, where 'required' is defined by the concentration in biomass which permits the organism to achieve its maximum metabolic and growth potential. In terms of number of atoms, H and O dominate through the occurrence of H2O as more than half of the biomass of essentially all organisms. On the basis of H20-free biomass H, C and O dominate, with N, P, K, S, Mg and Ca comprising the other 'major' essential elements. The other essential elements are needed in much smaller amounts (10~^-10"^ that of C).
Chemistry of the early oceans: the environment of early life
How could the early ocean supply energy for the origin and early evolution of life? Life requires a continual input of free energy for the growth and maintenance of organisms. The free energy transformed by organisms can, in principle, come from a very wide range of sources, for example mechanical energy (e.g. water flow over an attached organism) and osmotic potential energy (e.g. tidal changes in external salinity in an estuary). In the absence of significant evidence for such energy sources in extant organisms, we deal here with catalysis of the coupling of energy from light, or organic chemical, or inorganic chemical reactions, to essential processes in the origin of life, and the early evolution of life. In all cases energy is dissipated during the energy transformations; less energy is stored in the products than was present in the substrate if a net conversion of useful energy is to take place. In addition to coupling the exergonic reaction to the (pre)biologically significant endergonic reaction, catalysis is involved in speeding the exergonic reaction which is based on energetic disequilibrium. Dealing first with photochemistry, solar radiation is not, of course, endogenous to the sea. There is a very weak radiation, some of which is at wavelengths which could be involved in profitable photochemistry, in the ocean as a result at least in part of sonoluminescence involving thermal excitation of Na"^ ions (Matula, 1999; Hilgenfeldt et ah, 1999). However, it is not certain that the radiation is quantitatively sufficient to support photosynthetic life (see Yurkov and Beatty, 1998). Furthermore, it is likely that at least some of this radiation comes today from the spontaneous oxidation of sulfide by molecular oxygen (Tapley et al., 1999). This mechanism would not have been available to the earliest life forms with ready access to sulfide, especially at hydrothermal vents, but with negligible molecular oxygen available until biological production of this gas evolved. One of the inorganic sinks for this oxygen which delayed its accumulation in the biosphere was, of course, this photon-emitting oxidation of sulfide.
59
Solar radiation is clearly adequate to support photosynthesis amounting globally to some 4Pmol inorganic-C converted to organic-C each year in the present ocean (Falkowski and Raven, 1997; Table 4.2). However, this productivity is confined to the upper 300 m of even the most transparent seawater as a result of the photon absorption properties of H2O. Generally there are other absorbing and scattering materials in seawater which attenuate solar radiation and decrease the depth at which photosynthetic growth can occur. All natural waters, regardless of their O2 content, attenuate UV radiation more than photosynthetically active radiation (Kirk, 1994a, b). While photochemical energization of the earliest living cells is neither likely nor widely advocated, it is possible that photochemistry in the ocean, and especially in the atmosphere, was important in generating particular chemical species related to the origin of life. Turning to the energization of early life by organic chemical reactions (chemo-organotrophy), this requires a prebiotic generation of organic matter. This could result from atmospheric (energized by UV radiation, lightning or meteorite impacts), crustal (including hydrothermal vent/bulk seawater interactions, and reactions at the crust/seawater interface) or extraterrestrial (coming to Earth on comets) events. It also requires that some reaction of the organic substrate is exergonic, by an internal rearrangement of the organic substrate, including its dismutation, or by reaction with some other organic or inorganic molecule (see Broda, 1975). Current views are that this is not the most likely means of energizing the earliest cells (see Edwards, 1998). The third possibility is that the earliest cells were chemolithotrophic, i.e. were energized by inorganic chemical reactions. This currently popular hypothesis is supported by molecular phylogenetic evidence suggesting that the root of the universal tree of life is in extant chemolithotrophic (and thermophilic) organisms (Pace, 1997). Suggestions have been made of chemically (Wachterhauser, 1990) and geologically (Russell and Hall, 1997, 1999) explicit models of a chemolithotrophic energization of
60
Evolution
on Planet Earth
the origin of life and of the earhest organisms (Table 4.2). The chemically explicit models of Wachterhauser (1990) relate to surface chemistry in the Hadean Ocean which can drive reactions such as FeS + H2S + CO2 -^ FeS2 +HCC)OH, and subsequently the reactions of the reverse tricarboxylic acid cycle. Russell and Hall (1997, 1999) base their mechanism of energy transduction on the hotter, more reducing, more alkaline solution emanating from hydrothermal vents reacting with the warm, less reducing, less alkaline bulk seawater. The reaction is suggested to occur across an iron monosulfide layer which forms spontaneously between the two solu-
4.3 Billion years ago ^^•••'••'•^r^i.,,,.^.^^
tions. Russell and Hall (1997, 1999) suggest that this 'membrane' could act as the place in which exergonic redox reactions (more reducing inner phase, less reducing outer phase) and H"^ fluxes (from the less alkaline outer phase to the more alkaline inner phase) could energize essential biosyntheses. How this occurred, and how the iron monosulfide 'membrane' became a lipoprotein biological membrane, needs further clarification (see Blobel, 1980; Koch and Schmidt, 1991; Edwards, 1998; Russell and Hall, 1999). The Russell and Hall (1997, 1999) scheme for a chemolithotrophic origin of life is shown in Figure 4.1 in the context of Mars 4.3 billion years ago (Early Noachian). Atmosphere <10 bars of CO2 with CO, SO2 and N2 but very low O2
mmEmocEAM Hot-sprtr^
Volcanic oceanic crust (mafic/ultramafic)
5 km
Descending 1 ocean water
Alkaline hydrothermal solution 200°C PH
Oxidation Hydration .Carbonation -250°C
COp
1 mm
Figure 4.1 Model environment for the emergence of life on Earth or Mars (reproduced with permission from Russell, M.J. and Hall, Allen J. (1997/1999) On the inevitable emergence of life in Mars (Julian A. Muscot, ed.). The Search for Life on Mars. Proceedings of the 1st UK Conference, British Interplanetary Society, London) by chemolithotrophic mechanism, related specifically to the putative Early Noachian (Mars 4.3 billion years ago) ocean floor at a submarine alkaline hot spring. The mechanism proposes that the fatty acids which compose the organic membrane which replaced the iron monosulfide were generated in the iron monosulfide compartments comprising the sulfide mound.
Chemistry of the early oceans: the environment of early life This model of the energization of the early iron monosulfide 'membrane' and the early lipoprotein membranes in terms of an electrochemical potential gradient of H"^, involving chemiosmotic reactions (Koch and Schmidt, 1991; cf. Raven and Smith, 1981, 1982), is based on an early ocean which was acidic or near-neutral (Kasting, 1993; Russell and Hall, 1997, 1999). It is important to realize that there are alternatives to this notion of an acidic early ocean, e.g. the early soda ocean suggestions of Kempe and Degens (1985) and Kempe and Kazmierczak (1997). The suggestions as to the evolution of H"^ active transport across membranes and of chemiosmotic reactions of Raven and Smith (1981, 1982) were in fact based on a neutral or slightly alkaline early ocean, albeit not in the context of a chemolithotrophic origin of life and chemolithotrophic energization of the earliest cells. The lack of calcification of the earliest organisms accords better with an acidic rather than an alkaline early ocean. An acidic early ocean would, in equilibrium with more than 0.1 MPa partial pressure of CO2, have both a high concentration of CO2 (in excess of 40molm~^ CO2). There would also be a high concentration of HCOs", at least 4molm"^ with a pH of 5, i.e. at least twice the concentration in today's sea water with a pH of 8.0 in equilibrium with 33 Pa CO2 in the atmosphere. This high CO2 concentration in the early ocean (regardless of its pH, providing it is in equilibrium with at least 0.1 Ma CO2 in the atmosphere) would be adequate to saturate the carboxylase enzyme(s) of any known autotrophic or anaplerotic inorganic carbon fixation (Raven, 1991, 1997a, b, c). This conclusion is independent of whether the enzymes use CO2 or HCOs" as their immediate substrate (provided that the intracellular pH is maintained close to neutrality), or of whether there is a significant diffusion restriction of CO2 entry (Raven, 1991, 1997a, b, c). At all events, CO2 diffusion through water and the lipid component of lipoprotein bilayers would have been adequate to supply inorganic carbon to the carboxylases; no inorganic carbon concentrating mechanisms would have been needed.
61
Although much needs to be clarified, the chemolithotrophic energization of the earliest biota seems to be the best currently available hypothesis.
How did early biota cliange ocean cliemistry and how did these chemical changes influence the early evolution of life? We assume a chemolithotrophic origin of life, and chemolithotrophy as the earliest energetic coupling mechanism in biota. In quantitative terms it is likely that the rate of reductant input from hydrothermal vents would limit worldwide primary production each year to about SOGmole, at least inasmuch as input through vents is concerned (Jakosky and Shock, 1998). A parallel input of chemolithotrophic substrates could come from the sorts of reactions discussed by Wachterhauser (1990). However, quantifying the productivity based on such energization is more complex, and will not be attempted here. To this 'new' productivity could be added 'recycled' productivity, which could result from the regeneration of inorganic reductant and inorganic carbon from 'respiratory' metabolism of the organic carbon and inorganic oxidant generated in chemolithotrophy. Such cycles of recycled chemolithotrophic productivity and 'respirationbased' productivity would run down, for example by sedimentation of reactants such as organic carbon (and inorganic oxidant?). Thus there is likely to have been an incomplete recycling of the products of chemolithotrophy to regenerate reductant at a sufficient reducing redox potential to reduce inorganic carbon to sugars. However, additional productivity could result from an additional energy input which could generate a strong reductant from a weaker reductant. Such an energy input could come from photons in the process of photosynthesis, permitting growth by photolithotrophy. However, thus far we have been implicitly considering biota at great depth in the ocean, centred on hydrothermal vents. These biota would have not suffered from
62
Evolution on Planet Earth
damage from the higher than present UV output from the young Sun, unscreened by the atmosphere due to the absence of O2, and hence UV-absorbing O3, in the atmosphere, due to the great depth of UV-absorbing water (Kirk, 1994a). However, despite the lower attenuation of photosynthetically active radiation than of damaging (UV-B) UV radiation by natural seawaters as has been mentioned earlier, no photosynthetically significant radiation from the Sun penetrates to 300 m even in the clearest waters. As to why the biota should occur close enough to the ocean surface to permit photosynthesis, we can suggest that chemolithotrophs were exploiting inorganic reductants in near-surface sediments. A plausible model for the evolution of photosynthesis from UV-screening protein-pigment systems is given by Mulkidjanian and Junge (1997). Here the UV was screened out by absorption of UV by membrane-associated proteins, with associated pigments (cyclic tetrapyrrols) able to accept excitation energy transferred from the protein, with energy dissipation by fluorescence, heat or photochemistry. The photochemical option for dissipation of UV energy could generate a strong reductant from a weaker reductant. Eventually, the energization of this process came to rely almost entirely on the absorption directly by the tetrapyrrol pigments of longer wavelength (>400 nm) radiation. In such organisms the UV-screening protein-pigment complexes evolved independently into two kinds of reaction centers of the RCl and the RC2 types (Mulkidjanian and Junge, 1997). Both of these can bring about inorganic carbon reduction to sugars using reductant originally derived from weak reductants such as S^~. Ultimately even weak reductants such as Fe and S;'/-~ would be locally exhausted, as sedimentation of the organic product of primary production prevented the respiratory regeneration of Fe^"^ from Fe^"^ and S from S° and S04^~. Such local depletion of weak reductants means that continued photosynthetic generation of strong reductants which could reduce inorganic carbon to carbohydrates, required the substitution of an even
weaker reductant for the S^~ and Fe^"^. This even weaker reductant is H2O which is, for all biotic purposes, infinitely available in sea water. The energy required to move an electron from H2O to a reductant strong enough to reduce inorganic carbon to produce sugars is significantly greater than that needed for the use of a stronger reductant as electron donor. Accordingly all 02-evolving organisms (i.e. those using H2O as their electron donor) have both an RCl and an RC2 reaction involved in transferring an electron from H2O to CO2, so that the energy from two photons (one used in the RCl, the other in the RC2) is used to transfer the 'electron'. In evolutionary terms what is needed here is a horizontal gene transfer so that RCl and RC2 can be expressed in a single cell. Furthermore, the redox span covered by RC2 is shifted toward more oxidizing potentials, so that the oxidant generated by this RC2 can oxidize H2O to produce O2, but the reductant generated by this RC2 is certainly incapable of reducing inorganic carbon to sugars (Olson and Pierson, 1986; Trissl and Wilhelm, 1993). The remainder of the redox span to the redox level needed to reduce inorganic carbon to carbohydrates is covered by RCl. The ability to use H2O as the ultimate electron donor for inorganic carbon fixation, with consequent O2 production, increases the ability of photosynthetic organisms to oxidize the S^~ and Fe^"^ in the ocean over and above the direct oxidation of S^" and Fe^"^ by organisms with RCl or RC2. O2 build-up in the atmosphere requires that the O2 produced in photosynthesis is not entirely consumed in respiration of the other product of photosynthesis, i.e. organic carbon sedimentation and long-term storage of this organic carbon is needed. O2 accumulation in the atmosphere also requires that the S^~ and Fe^"^ sinks for O2 have been oxidized; these S^~ and Fe^"^ sinks are not just the pre-existing pools in the ocean, but also the continued input from hydrothermal vents. Finally, the presence of O2 in the atmosphere permits oxidation of Fe^"^ and S^~ exposed on the continental crust, first found some 3.5 billion years ago (Buick et al., 1995; Raven, 1997a), again forming a sink for O2 which must be satisfied before O2 can further increase in the atmosphere.
Chemistry of the early oceans: the environment of early life The build-up of O2 would diminish the availability of Fe and Mn to 02-evolving photosynthetic organisms due to the insolubility of the Fe203 and Mn02 which form under oxidizing conditions. However, Cu becomes much more available under these conditions, as the soluble Cu^"^ instead of the very insoluble CU2S. The implications of this for the functioning, and subsequent evolution, of photosynthetic 02-evolvers is discussed by Raven et al. (1999). Furthermore, organic matter can scavenge Mo from seawater, thus providing another feedback of the evolution of life on the chemistry of the oceans, in this case with implications for the capacity of organisms to acquire N for N2 and NO^ via Mo-requiring nitrogenase and nitrate reductase enzymes (Holland et al, 1986; Falkowski, 1997; Falkowski and Raven, 1997).
Conclusion The early ocean provided all of the elemental requirements for the origin and early evolution of life, although some inputs from the atmosphere and crust were needed to provide the appropriate chemical species. The chemistry of life is determined by both the appropriate chemical properties of a given element and its availability. Some essential elements (e.g. P) may not have been abundant at any stage during the origin and early evolution of life. Inorganic chemical reactions are the only energy sources for the origin of life which are endogenous to the early ocean, especially if the crust/ocean interface is acceptable as part of the ocean. These inorganic chemical energy sources (e.g. involving Fe and S) could allow a chemolithotrophic energization of the origin and early evolution of life. Additional energy inputs could come from the more alkaline and reducing solution from hydrothermal vents which is out of energetic equilibrium with the less alkaline, less reducing, seawater. Early life modified the chemistry of the early ocean. In conjunction with the sedimentation of organic reduced products of chemolithotrophs (and possibly of the oxidized inorganic pro-
63
duct), chemolithotrophy would decrease the availability of inorganic reductant for chemolithotrophy. This modification to the medium, together with use of some of the metabolic machinery involved in chemolithotrophy, provides both selection pressure and some part of the mechanism for the evolution of photolithotrophy.
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