Emerging Views on the Evolution of Atmospheric Oxygen During the Precambrian 185

184 Journal of Mineralogical andB. Petrological Sreenivas and Sciences, T. Murakami Volume 100, page 184─ 201, 2005 Emerging views on the evolution of atmospheric oxygen during the Precambrian 185

Emerging views on the evolution of atmospheric oxygen during the Precambrian

*,** * Bulusu SREENIVAS and Takashi MURAKAMI

*Department of Earth and Planetary Sciences, Graduate School of Science, The University of Tokyo, 7－3－1 Hongo, Bunkyo－Ku, Tokyo 113－0033, Japan ** Permanent address: National Geophysical Research Institute, Hyderabad 500007, India

The oxygenation of the atmosphere produced some irreversible changes in the Earth’s history, including evolution of higher biological forms. Several aspects of this important process, such as its timing and causes, have remained subjects of debate. The present review is an attempt to provide an update on issues related to the evolution of atmospheric oxygen during the Precambrian. It is generally believed that the amount of atmospheric oxygen increased during the Paleoproterozoic despite the fact that photosynthesis originated much earlier in the Earth’s history. The pattern of Fe retention in paleosols and the record of mass－independent fractionation in sulfur isotopes confirm that the transition to more oxidizing conditions took place during the Paleoproterozoic. Various mechanisms, ranging from an increase in the sources of oxygen to a decrease in its sinks, have been envisaged as processes causing the oxygen rise during the Paleoproterozoic. Conventionally, it is believed that the burial of photosynthetic carbon has allowed the establishment of oxygen. However, the transition in mantle oxidation states and the escape of hydrogen during photolysis of methane of biogenic origin have also been suggested as having played an important role in the establishment of free molecular oxygen in the atmosphere－hydrosphere system. The coincidence of timing of the oxygen rise and the positive excursions in carbon isotope compositions of carbonate rocks during the Paleoproterozoic suggests an important role for the carbon cycle in atmospheric oxygen evolution. Better quantitative modeling of atmospheric oxygen levels may be essential to allow full comprehension of the timing, causes and consequences of the oxygen rise in the Earth’s history. Quantitative modeling is essential as it can lead to an unraveling of the co－evolutionary nature of the surface environment and the biosphere of the Earth.

Keywords: Precambrian, Atmosphere, Oxygen, Evolution

INTRODUCTION 1995). The history of atmospheric oxygen evolution war- The accumulation of free molecular oxygen in the atmo- rants at least two changes necessitated by the biological sphere－hydrosphere system at some time during the evolution during geological history. Firstly, the atmo- −3 Precambrian has enabled aerobic life to be sustained on spheric PO2 had risen from low values to ≥ 2 × 10 atm by the surface of the Earth, triggering a fundamental change the time the eukaryotes were stabilized, as they would in the way the biosphere evolved. This has laid the foun- require 10% of the present atmospheric level (PAL) dation for the current shape and status of the Earth sur- (Runnegar, 1991). The next rise in PO2 should be up to face. The possible critical role of atmospheric oxygen lev- ~ 50% PAL, which is the limit required by animals els on the evolution of complex multicellular life suggests (Runnegar, 1982; Knoll, 1992). Both the pattern and the co－evolutionary nature of the life and environment on underlying causes of the oxygenation events have Earth (Hedges et al., 2004). Understanding the evolution remained highly debatable. Models of atmospheric oxy- of atmospheric oxygen is therefore regarded as a funda- gen evolution show wide variation regarding the timing mental problem of Earth sciences (Knoll and Holland, and pattern, as summarized in Figure 1. Because of the lack of direct methods (Holland, B. Sreenivas, [email protected] 1994), it is difficult to estimate the composition of the T. Murakami, [email protected]－tokyo.ac.jp Corresponding author Precambrian atmosphere, and information regarding the 184 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 185

Figure 1. Various models of atmospheric oxygen evolution based mainly on the compositions of paleosols and the record of mass independent isotope fractionation in S isotopes during the late Archean to Paleoprotero- zoic. The main discrepancy is between

the high PO2 model throughout the Precambrian and those indicating a drastic rise during the Paleoprotero- zoic.

atmospheric oxygen content has always been sought from the following sections, we discuss the status of various secondary sources. Much information from geological, indicators such as banded iron formations (BIFs), red mineralogical and geochemical research has been used to beds, detrital heavy minerals (uraninite, pyrite, etc.), sul- deduce information regarding oxygen levels of past atmo- fates, paleosols and stable isotope records of carbon, sul- spheres. Essentially, the secular variation of redox－sensi- fur and nitrogen, all of which have been used to deduce tive signatures in the geological record has been used for the timing of the oxygen rise. this purpose. Despite numerous attempts, unequivocal solutions to this most critical problem still appear highly Banded iron formations (BIFs) and red beds elusive. In this review, an attempt has been made to present recent updates on various matters associated with the The Precambrian record of BIFs presents a unique fea- timing, causes and consequences of atmospheric oxygen ture: deposition of such formations is completely absent rise during the Precambrian. The subsequent sections over the billion years of Earth history starting from ~ 1.8 have been organized into three main topics of discussion Ga (Fig. 2) (Cloud, 1972, 1973; Klein and Beukes, 1992). surrounding the timing, causes and consequences of the Cloud (1972) believed that the cessation of BIF deposi- atmospheric oxygen rise. tion at ~ 1.8 Ga marked the end of an anoxic regime and a great oxidation event brought about irreversible and dras- TIMING OF ATMOSPHERIC OXYGEN RISE tic changes around this time. Although they are anoma- lously absent from ~ 1.8 Ga, BIFs are consistently present Various indicators in the geological and geochemical in the geological record from the earliest Archean. All records have been used to pin down the exact timing of Precambrian BIFs, including the oldest (~ 3.8 Ga) one the atmospheric oxygen rise during the Precambrian. The from Akilia, Greenland (Dauphas et al., 2004), seem to hypotheses regarding the timing of the oxygen rise fall into two broad categories (Fig. 1). Many lines of evidence have been presented to suggest that the rise in atmospheric oxygen levels—termed the Great Oxidation Event (GOE, after Holland, 2002)—took place some time during the Paleoproterozoic (2.3 to 1.8 Ga) (Cloud, 1968, 1972, 1973; Walker, 1977; Walker and Brimblecombe, 1985; Kasting, 1987; Holland, 1984, 1994, 1999). Contra- dicting this, it is also proposed that atmospheric oxygen reached high levels and remained constant from the early Archean (from about 4 Ga) onwards (Dimroth and Kimberley, 1976; Clemmey and Badham, 1982; Towe, 1990; Ohmoto, 1992, 1996, 1997, 2003, 2004; Watanabe Figure 2. The distribution of BIF deposits during the Precambrian. et al., 1997, 2000, 2004; Lasaga and Ohmoto, 2002). In Note the long pause in BIF deposition between 1.8 and 0.8 Ga. 186 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 187 have been formed by the generation of ferrous iron close to mid－ocean ridges and its deposition near the shore after oxidation to the ferric state. The time when formation of BIFs ceased has been correlated with the time when ocean water was oxidized and removed ferrous iron. It was earlier thought that the time period witnessing the disappearance of BIFs also marked the appearance of red beds, which suggests surface oxidizing conditions (Cloud, 1972). These simultaneous phenomena—disappearance of BIFs and appearance of red beds—appealed as very compelling evidence for a widespread oxidation of the Figure 3. Secular variation in Eu anomalies (the behavior of Eu with respect to neighboring REEs) of BIF deposits. The Eu anom- Earth’s surface at ~ 1.8 Ga (Cloud, 1972). However, sev- * alies are calculated using the equation Eu/Eu = EuN/√SmN × GdN, eral later pieces of evidence, including the earlier appear- where subscript N denotes the normalized values. The REE com- ance of red beds, suggested that the rise in oxygen con- positions have been normalized to the oxide facies Hamersley centration had been initiated by ~ 2.2 Ga, some 0.4 Ga BIF deposits. Barring the ~ 2.7 Ga BIF deposits (showed in open earlier than the time indicated by the BIF－red bed phe- squares), a gradual decrease in Hamersley－normalized Eu anom- nomenon (e.g., Holland, 1994). This led to the supposi- alies with time can be observed. tion that the pattern of BIF abundance may not reflect the change of surface oxidation conditions and may simply porally and spatially connected equivalents in the point to the time of oxidation of the deep ocean (Ohmoto, Transvaal Supergroup of South Africa, represent more 1997). than 70% of total BIF deposits (Isley, 1995). These ~ 2.45 Some secular variations in the characteristics of BIFs Ga BIFs represent an intense phase of hydrothermal activ- are worth mentioning in relation to the understanding of ity related to a global mafic magmatic event (Barley et al., atmospheric oxygen rise. On the basis of the control of 1997; Heaman, 1997) and, hence, hydrothermal effects on depositional settings in BIF mineral assemblages, Beukes the REE signatures of these BIFs should also be at a max- and Klein (1990) suggested that the shallow water facies imum. When normalized to Hamersley compositions, any BIF deposits of > 2.45 Ga were deposited under reducing deviations in Eu or Ce anomalies in older or younger conditions, whereas those of < 2.2 Ga are thought to have BIFs should reflect conditions other than hydrothermal been deposited under oxidizing conditions (Beukes and nature. The Eu anomalies of the Precambrian BIFs are Klein, 1992). The changes in rare earth element (REE) plotted in Figure 3. It can be seen that, with the exception compositions of BIFs, mainly the positive Eu and nega- of 2.7 Ga old BIFs, the rest show a gradual decrease in Eu tive Ce anomalies, were initially considered as possible anomalies (Fig. 3), which is very similar to the observa- indicators of evolving redox states of shallow water depo- tion made by Condie (1997) on BIFs and cherts. All the sitional conditions (Fryer, 1977). It has been shown that pre－2.45 Ga BIFs are characterized by positive Eu anom- the BIFs older than 1.9 Ga age are more enriched in Eu alies whereas the younger ones are negative. We suggest than the neighboring REEs. This indicates that consider- such a gradual change may reflect shallow water gradu- able amount of Eu has remained as Eu2+ during the pro- ally becoming oxygenated. However, such variation of Ce cesses of weathering－transportation－deposition, which anomalies with time has not been observed. The presence suggests more reducing conditions during that period of negative Ce anomalies in ~ 2.9 Ga BIFs has been inter- (Fryer, 1977). However, with the affirmation of hydro- preted to represent oxygenated deep ocean water condi- thermal sources for Fe as well as REEs in all the BIFs tions (Kato et al., 2002; Ohmoto, 2004). (Jacobsen and Pamintel－Klose, 1988), the redox evolu- One of the emerging views suggests that the cessation was decoupled from the REE characteristics of BIFs. tion of BIF deposition at ~ 1.8 Ga may actually mark the Despite the fact that all the BIFs are of hydrothermal ori- transition of deep oceans to sulfidic conditions rather than gin, the positive Eu anomalies in them show a gradual oxic as a consequence of the 2.3－2.0 Ga oxidation event decrease from Archean to Proterozoic (Fryer, 1977; (Canfield, 1998). The BIFs may still yield some important Condie, 1997). We compiled the REE data of many Pre- answers in solving the timing and pattern of oxygen evo- cambrian BIFs and tried to test the changing nature of Eu lution during the Archean－Proterozoic transition, because and Ce anomalies with time (Fryer, 1977; Condie, 1997). the presence of vast amounts of Fe as a reductant in We normalized the REE compositions of all the BIFs to Precambrian seawater should have had great control on the oxide facies BIFs of the Hamersley Group of Western the oxygen levels of the atmosphere－hydrosphere system. Australia. The Hamersley BIFs, together with their tem- The appearance of red beds is now considered to be 186 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 187

a Paleoproterozoic phenomenon, although Ohmoto (1997) alization is represented by the deposits of Oklo, Gabon, points to older occurrences. They start to appear in se- which are also called natural nuclear fission reactors quences of < 2.25 Ga from South Africa (Eriksson and (Gauthier－Lafaye and Weber, 1989). The U mineraliza- Chiney, 1992), Canada (Chandler, 1980) and the Fenno- tion has been dated to be ~ 1.95 Ga, whereas the sedi- scandian shield (Holland, 1994). The appearance of Mn ments hosting them are ~ 2.15 Ga (Gauthier－Lafaye and formations in the geological record can also be taken as Weber, 2003). This mineralization event postdates the Mn good evidence for the oxygen rise, as the oxidation of Mn deposits present in the sequence. Based on the Mn forma- requires molecular oxygen or nitrate (Kirschvink et al., tions and U mineralization in this Paleoproterozoic series,

2000). It has been suggested that Mn deposition is inhib- it has been postulated that a major transition in PO2 took ited by the presence of Fe in the water column (Roy, place between 2.15 and 1.95 Ga (Gauthier－Lafaye and 2000). The deposition of the world’s largest Kalahari Mn Weber, 2003). formation in the Transvaal Supergroup, South Africa by ~ 2.25 Ga has been taken as evidence of the atmospheric Redox-sensitive elements and isotopes in shales oxygen rise accompanying the global glaciation events

(Kirschvink et al., 2000). However, the late Archean for- The Fe2O3/FeO ratios, Mo, U and Re abundances, and mations of India and Brazil may point otherwise (Roy, Re－Os isotope compositions of shales have been utilized 2000). to infer the secular change in oxidative conditions of the

atmosphere. It has been shown that the Fe2O3/FeO ratios Detrital uraninite, pyrite and siderite of 2.3－2.1 Ga old shales are distinctly high compared with those of shales aged > 2.3 Ga (Bekker et al., 2003). Presence of detrital uraninite and pyrite in the late The mobility of redox－sensitive trace elements such as Archean quartz pebble conglomerates of South Africa Mo, U and Re is sensitive to the presence of oxygen. (Ramdohr, 1958), Canada (Roscoe, 1969) and southern These elements are mobilized under oxidative weathering India (Srinivasan and Sreenivas, 1968) has been consid- conditions and their concentrations in marine shale should ered strong and direct evidence for an anoxic Archean therefore mark the transformation in oxidative conditions atmosphere (Grandstaff, 1980; Holland, 1984). However, (Yang and Holland, 2002). It has been found that the con- the detrital origin of these heavy minerals has been ques- centrations of Mo, U and Re in carbonaceous shales of tioned and a hydrothermal origin has been proposed > 2.0 Ga are not correlated with the organic carbon con- (Barnicoat et al., 1997; Philips and Law, 2000). Further, tent, whereas those of ~ 1.6 Ga show characteristics simi- Ohmoto (1997, 2004) questioned the validity of the detri- lar to modern shales, which indicates that oxidative tal heavy minerals as indicators of redox conditions, weathering was established by this time (Yang and pointing out that their occurrence is restricted to poorly Holland, 2002). In another study, it has been suggested sorted fluvial sediments. Recently, it has been shown that that the Archean and Paleoproterozoic shales are charac-

the middle to late Archean fluvial sediments of the Pilbara terized by lower Mo/Corg values than the Phanerozoic craton of Australia have preserved definite uraninite, ones, and the Mo cycle during the Precambrian was pyrite and gersdorffite as well as siderite (Rasmussen and largely controlled by the redox structure of the oceans and Buick, 1999). Further, England et al. (2002) have shown may not have a direct implication for the oxidation state that the pyrites in the Witwatersrand Supergroup are of the atmosphere (Yamaguchi and Ohmoto, 2002). indeed of detrital origin, based on their petrographic and Osmium isotope ratios of the Archean to Paleoproterozoic sulfur isotope analysis. It has been shown that uraninite shales, similar to those of chondrite, are consistent with － and pyrite are kinetically stable under PO2 conditions of oxygen deficient conditions (Hannah et al., 2004a, < 0.1 and 0.01 PAL, respectively (Ono, 2001). It may not 2004b). The behavior of U, using Pb isotope systematics

be possible to quantify the atmospheric PO2 on the basis of to overcome the metamorphic/metasomatic effects, has the presence of detrital placers (Holland, 1984) but, based been assessed in the late Archean to Paleoproterozoic on their definite presence, anoxic conditions may be shales and suggests the onset of oxidative weathering inferred during the Archean (Holland, 1999). conditions by ~ 2.2 Ga (Jacobsen et al., 2004). Oxidizing ground water started playing a major role Trace element patterns in rocks derived from the during the Proterozoic and the style of U mineralization mantle have also been utilized to understand the evolution was accordingly changed. Under oxidizing conditions, of redox conditions during the Precambrian (Collerson U(IV) is unstable and is oxidized to U(VI), which is solu- and Kamber, 2000). It has been shown by these authors ble in water and can be transported along with water (e.g., that a smooth decrease in Th/U ratios and a kink in Nb/U Langmuir, 1978). The major Proterozoic type of U miner- ratios of mantle－derived rocks had started at ~ 2 Ga and 188 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 189 may be related to the timing of atmospheric oxygen rise. The relative increase of U may have occurred because U(VI) mobilized under oxygenated conditions was incorporated in marine sediments and then accumulated into the mantle through subduction (Collerson and Kamber, 2000).

Paleosols

Paleosols, soils of the geological past, have been recognized long ago as important indicators of atmospheric oxygen as they develop at the interface of the lithosphere Figure 4. Gradual increases in Fe and Mn retention factors (fractions retained in the paleosol profiles represented as Fe2O3(T)R and and atmosphere (Holland, 1984). In fact, paleosols are the MnOR, respectively) of late Archean to Paleoproterozoic paleo- only candidates that yield semi－quantitative information sols (Sreenivas et al., 2004). Near complete retention of both Fe on the atmospheric oxygen levels during the Precambrian and Mn is observed only in the ~ 1.85 Ga Flin Flon paleosols of (Rye and Holland, 1998 and references therein). The esti- Canada. mation of PO2 using paleosol compositions has been carried out by comparing the Fe content in paleosol and par- thus more appropriate for such estimation. The Fe and Mn ent rocks and converting them into the demand of O2 and oxide retentions gradually increase with age and both Fe

CO2 during weathering (Holland, 1984). An initial model and Mn have become immobile only in 1.85 Ga old Flin of a drastic rise in atmospheric oxygen from ≪ 10−3 to Flon paleosol (Fig. 4). The significant loss of Fe in paleo- > 10−3 atm has been constructed using mainly data derived sols of 2.7 and 2.45 Ga indicates oxygen－poor conditions, from paleosols (Holland and Buekes, 1990). Rye and as suggested by the experiment to constrain the Fe behav- Holland (1998) subsequently reviewed the geochemical ior during biotite dissolution under anoxic conditions data of all the well－preserved Precambrian paleosols and (Murakami et al., 2004a). The Fe distribution pattern in proposed that they are consistent with a drastic rise in PO2 ferrous and ferric forms in the 2.45 Ga old Cooper Lake from ~ 10−4 to 0.1 atm between 2.2 and 2.0 Ga (Fig. 1). It paleosol has been suggested as possible under anoxic is also pointed out that the 2.25 Ga Hekpoort paleosol of weathering conditions (Utsunomiya et al., 2003). Com- South Africa represents the last of the paleosols from plete Fe retention has been observed in paleosols < 2.25 which Fe has been removed during weathering (Rye and Ga, indicating an oxygen rise between 2.45 and 2.25 Ga. Holland, 2000a). On the other hand, pointing to the possi- The suggested similarities of characteristics between bility of remobilization of Fe by reducing metasomatic weathering profiles of 2.25－2.0 Ga and modern laterites alteration or organic acids, Ohmoto (1996) questioned the (Gutzmer and Beukes, 1998; Beukes et al., 2002) indicate significance of paleosols as barometers of atmospheric complete Fe retention in < 2.25 Ga paleosols. On the oxygen, and suggested that the PO2 has remained high and other hand, a much earlier origin for highly oxidative con- constant (~ 50% PAL) at least since the early Archean. In ditions including terrestrial biota has been proposed on addition, based on the analyses of the Gaborone section the basis of elemental distribution in Precambrian paleo- (Zimbabwe) of the Hekpoort paleosol, two independent sols (Ohmoto, 1996; Watanabe et al., 2004) and carbon studies have shown that the Hekpoort paleosol, of which isotope analysis in Kalkkloof and Schagen paleosols of the upper portion is rich in Fe, is similar to modern later- ~ 2.65 Ga age (Watanabe et al., 2000). It may be pointed ite and the earlier－analyzed eastern sections of the out here that very light carbon isotope compositions in the Hekpoort paleosol are representative of soils affected by carbon associated with ~ 2.7 Ga old Mt. Roe paleosols erosion (Beukes et al., 2002; Yang and Holland, 2003). have been attributed to methanotrophs of ephemeral To overcome the problems associated with erosional ponds (Rye and Holland, 2000b). losses, estimation of retention factors of Fe and Mn in The abundances and ratios of REE in Precambrian Precambrian paleosols on an isovolumetric basis has been paleosols have been utilized to understand redox condi- carried out using geochemically derived compaction fac- tions of the atmosphere (Macfarlane et al., 1994; Panahi tors (Sreenivas and Das Sharma, 2002; Sreenivas et al., et al., 2000; Pan and Stauffer, 2000; Murakami et al., 2004). Sreenivas and his co－workers used the late 2001; Sreenivas et al., 2001a; Utsunomiya et al., 2003; Archean to Paleoproterozoic paleosols that had formed on Nedachi et al., 2005). Rhabdophane, a secondary mineral basaltic parent rocks, because basaltic rocks are more formed by weathering with almost all Ce as Ce(III), was homogeneous and richer in Fe than granitic rocks and first found in the Pronto paleosol of Canada (Murakami et 188 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 189

Figure 5. Ce anomalies in the late Archean to Paleoproterozoic paleosols. The Ce anomalies are calculated using the equation * Ce/Ce = CeN/√LaN × PrN. The REE compositions of the paleosol samples have been normalized to chondrite compositions. Note the positive Ce anomalies in the Flin Flon paleosols only corrob- orating with the Fe and Mn retention patterns. Figure 6. Variation in carbon isotope composition of carbonate car- 13 bon (δ Ccarb) as a function of the fraction of buried organic car- 13 13 bon calculated using the mass balance equation δ Cin = δ Ccarb al., 2001). The REE patterns (Ce/La ratios) of rhabdo- 13 (1 − ƒorg) + δ Corg (ƒorg) (Des Marais et al., 1992; Schidlowski phane provide direct evidence of an oxygen－deficient 13 13 and Aharon, 1992). Values of δ Cin and δ Corg are taken as −5 13 atmosphere during the late Archean to earliest Paleo- and −25‰, respectively and the δ Ccarb values are estimated as a proterozoic period. Pan and Stauffer (2000) have shown response to increases in ƒorg values using the above mass balance 13 that ~ 1.85 Ga Flin Flon paleosols have been character- equation. The δ Ccarb values of global mean (0‰) and that of the ized by positive Ce anomalies, consistent with the obser- Paleoproterozoic maximum (12‰) are also plotted. Note that an enhancement in organic carbon burial will result in 13C－enrich- vation that both Fe and Mn have been retained in these ment in the carbonate carbon, considering no variations in the 13 13 Flin Flon paleosols (Sreenivas et al., 2004). We have plot- δ Corg and a constant δ Cin. ted the Ce anomalies in definite paleosols ranging in age from late Archean to Paleoproterozoic in Figure 5, where positive Ce anomalies of > 1.5 are observed only in 1.85 oxygen in the atmosphere－hydrosphere because most of Ga old paleosols. In an ongoing study on REE patterns of the photosynthetically generated oxygen is otherwise con- rhabdophanes from several late Archean to Paleopro- sumed by organic carbon. Positive excursions in the terozoic paleosols, it has been observed that there is a global δ13C record may thus reveal events of enhanced gradual decline in Ce/La ratios (Murakami et al., 2004b). organic carbon burial (Kaufman, 1997) and thereby This indicates that the atmospheric oxygen rise was grad- increased release of oxygen to the atmosphere (Karhu and ual rather than drastic during the Paleoproterozoic—a Holland, 1996). The long－term variation in the carbon proposition in consonance with the observed patterns of cycle as revealed by the δ13C record of the carbonate Fe and Mn retention in paleosols. rocks is thus considered very important for understanding the geological controls on the evolution of the atmo- Carbon isotopes and biogeochemical cycle sphere, hydrosphere and biosphere. Initially it was believed that the sedimentary carbon- The carbon isotope composition (δ13C) of sedimentary ate record of both the Precambrian and Phanerozoic is carbonate is largely determined by the fraction of organic characterized by carbonate and organic carbon with rela- carbon accumulated along with the sediments, because of tively constant isotopic compositions of 0 and −25‰, the affinity of the lighter carbon isotope 12( C) towards the respectively (Keith and Weber, 1964; Schidlowski et al., organic form as a result of the kinetic isotope effect 1975). Based on the above observations it was inferred － (Schidlowski and Aharon, 1992). Enhanced burial of a that the increase in PO2 of the atmosphere is a steady state

fraction of organic carbon (ƒorg) will result in positive process, and the present oxygen level has been attained excursions in the δ13C value of sedimentary carbonate through cumulative processes over the 3.8 Ga of Earth’s rocks if the isotope compositions of input (mantle) carbon sedimentation history (Broecker, 1970). However, it has and the fractionation associated with the fixation of car- been found that many Precambrian carbonate sequences, bon into organic matter remain constant, as explained in especially those belonging to the Paleo－ and Neopro- Figure 6. Importantly the enhancement in organic carbon terozoic periods have been characterized by higher inci- burial also leads to the accumulation of free molecular dences of both enrichment and depletion in their carbon 190 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 191

changes in biological evolution. It is pointed out here that the appearance of eukaryotes by ~ 2.1 Ga may also indicate the timing of the oxygen rise. Both the causes and effects of these carbon cycle phenomena are still actively debated, although it is increasingly recognized that the 2.22－2.06 Ga excursion in δ13C values are global in nature and have profound significance for both atmosphere and hydrosphere evolution. Furthermore, preservation of many geochemical signatures that indicate a more complete oxygenation by ~ 1.84 Ga (Sreenivas et al., 2004)

13 suggests that the carbon cycle is central to the understand- Figure 7. δ Ccarb record during the Proterozoic showing positive excursions at the beginning (2.45－1.9 Ga) and end (0.8－0.54 Ga) ing of atmospheric oxygen evolution. stages. The positive excursions of questionable global origin during the Paleoproterozoic are shown accordingly. Sulfates and sulfur isotopes isotope compositions (Kaufman, 1997). The carbon iso- It has been suggested that pyrite is stable under very low tope record during the Proterozoic is plotted in Figure 7. atmospheric PO2 conditions (< 0.01 PAL; Canfield et al., 13 A positive excursion in Paleoproterozoic δ C values (up 2000; Ono, 2001). A slight increase in the PO2 value may to +12‰) was first observed in the carbonate rocks from affect oxidation of pyrite to form more soluble sulfate and the Fennoscandian shield of Russian Karelia (Schidlowski promote its runoff to the oceans. Since atmospheric oxy- et al., 1975; Galimov et al., 1975) and from the Loma- gen is the primary control on the input of sulfates to the gundi province of Zimbabwe (Schidlowski et al., 1976). oceans, the period of appearance of sedimentary marine These anomalous isotopic records initially were consid- sulfates may indicate the initial rise in atmospheric oxy- ered to be of local significance. However, it has been gen (Canfield, 1998). Sulfates start appearing in sedimen- found in the last few years that 13C enrichment is common tary sequences by ~ 2.2 Ga, as observed in Canada in carbonate rocks of 2.2－2.06 Ga old sequences from (Chandler, 1988) and Australia (El Tabach et al., 1999). northern Europe, North America, South Africa, Australia The world’s largest bedded barite deposit from the and India (Karhu and Holland, 1996; Melezhik et al., Cuddapah Supergroup of southern India (Neelakantam, 1999). Such a worldwide occurrence of 13C－enriched car- 1987) may also belong to the Paleoproterozoic age bonate rocks indicates the global nature of Paleopro- (Zachariah et al., 1999). The presence of evaporitic sul- terozoic δ13C excursions. This global excursion must have fates by 3.5 Ga is supposed to indicate the presence of resulted from a major disturbance in the carbon biogeo- locally nonreducing conditions (Nisbet and Sleep, 2001). chemical cycle and so is related to the evolution of the Importantly the enrichment of sulfate would have also atmosphere, hydrosphere and biosphere during the Paleo- promoted bacterial sulfate reduction and consequent sul- proterozoic. fur isotope (δ34S) compositional differences between Discrete and multiple δ13C excursions, associated coexisting marine sulfate and sulfides (Canfield and with glacial deposits aged between 2.43 and 1.93 Ga, Teske, 1996; Canfield, 1998). Ohmoto (1992) earlier have been identified in the Paleoproterozoic Transvaal observed that the Archean oceans contained sulfate levels and Olifantshoek Supergroups of South Africa (Buick et up to 30% of present day values since at least 3.5 Ga al., 1998; Bekker et al., 2001). The pattern of δ13C excur- onwards, based on the S isotope record of individual sions, together with glacial events, is strikingly similar to pyrite grains, and therefore he inferred that there were that in the Neoproterozoic carbonate sequences deposited higher free molecular oxygen levels from the Earth’s early between 0.85 and 0.55 Ga (Kaufman and Knoll, 1995). history. This suggests that the carbon cycle might have played a Subsequently, Canfield (1998) pointed out that the major role not only in oxygenating the atmosphere but difference between δ34S values of seawater sulfates and also in bringing about long－term climatic excursions, at sedimentary sulfides of possible bacterial origin started to least during the last two billion years (Des Marais et al., increase from ~ 2.2－2.3 Ga onwards, as shown in Figure 8, 1992; Kaufman, 1997). Megascopic eukaryotes that re- indicating the timing of the oxygen rise. The interesting quire high PO2 appeared in 2.1 Ga old Michigan BIFs (Han proposition coming out of this sulfur biogeochemistry is and Runnegar, 1992), which further implicates the role of that the deep oceans might still have been oxygen defi- the carbon biogeochemical cycle in oxygenating the cient following the cessation of BIF deposition at ~ 1.84 atmosphere, inducing climatic variations and affecting Ga and would have became sulfidic instead (Canfield, 190 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 191

34 Figure 8. Difference in the δ S values of coeval marine sulfates Figure 9. ∆33S variations with time showing a wide range of values and sulfides during the Precambrian. The shaded region indicates during the Archean, and this mass－independent isotope fraction- 34 － 34 the actual range of values δ Ssulfate δ Ssulfide at a given period. ation in sulfur isotope starts diminishing during stage II (after Note that > 20‰ values (indicated by the dashed line) start Farquhar et al., 2000; Farquhar and Wing, 2003). The filled circle appearing from ~ 2.3 Ga onwards. The sulfur isotope data plotted indicates the timing of initial rise in atmospheric oxygen at ~ 2.32 in the figure are taken from Canfield (1998). Ga (Bekker et al., 2004).

1998). The enhanced sulfide concentration resulting from and ozone concentrations (Fig. 9; Farquhar et al., 2000, bacterial reduction of sulfate, rather than oxygen, might 2001). Ultraviolet (UV) radiation experiments (Farquhar have removed Fe from deep ocean water. It is now pro- et al., 2001) and modeling (Pavlov and Kasting, 2002) on

posed that the deep oceans have remained anoxic during SO2 suggest that the UV transparency influenced the MIF the entire Mesoproterozoic from 1.84 Ga onwards, and in S isotopes. The data compilations of MIF in S isotopes that the cessation of BIF formation at this time is a reflec- over the Precambrian period suggest the following: a) the

tion of dominance of the sulfur cycle as a consequence of Archean (> 2.45 Ga) period is characterized by a PO2 of － −5 −5 −2 an initial rise in atmospheric oxygen at ~ 2.2 2.3 Ga. ≪ 10 PAL, b) the PO2 ranges between 10 and 10 PAL － −2 O Recent elemental and isotopic studies on the sedimentary during the period 2.45 2.0 Ga, and c) a P 2 > 10 PAL rocks of < 1.84 Ga attest to the dominance of a sulfide－ characterizes the < 2.0 Ga atmosphere (Farquhar and rich deep ocean (Shen et al., 2003; Arnold et al., 2004; Wing, 2003). Further, recent data from the Transvaal Poulton et al., 2004). This further sets the upper limit to Supergroup indicates that the oldest samples without any the extent of the initial oxygen rise during the Paleopro- MIF in their S isotope compositions (Δ33S = 0‰) are 2.32 −5 terozoic to be < 0.07 atm (30% PAL) PO2, as this is the Ga, which marks the time of the initial PO2 rise from < 10 minimum amount required for oxygenation of deep ocean to > 10−5 PAL (Bekker et al., 2004). It must be pointed out waters (Canfield, 1998). Based on the difference in the here that Δ33S values of > 0 ± 0.2‰, which are similar to δ34S values of > 45‰ V－CDT between sulfates and sul- those in the Archean sediments, have been found in vol- fides during the Neoproterozoic period, it is proposed that canic sulfates of South Pole glaciological records

a second oxygenation event caused the atmospheric PO2 (Savarino et al., 2003). This shows that processes other increase and deep ocean oxidation during the 0.8－0.54 Ga than UV transparency can also affect the MIF in S iso- period (Fig. 8; Canfield and Teske, 1996). The prolonged topes. It has also been argued that the observed MIF in S anoxic condition of the deep ocean for almost a billion isotopes may be due to analytical processes and compari- years, from 1.84 to 0.8 Ga, has significance in relation to son of MIF in organic carbon rich pyrites with sulfates primary organic productivity as well as algal evolution may not yield realistic variations (Ohmoto et al., 2001). during this period (Anbar and Knoll, 2002; Poulton et al., 2004). Nitrogen isotopes The discovery of mass－independent isotope fractionation (MIF) in sulfur isotopes, expressed as Δ33S ≠ 0‰ It has been shown that the δ15N values of the early and Δ36S ≠ 0‰, in Archean sediments and its absence in Archean organic matter are highly negative when com- Proterozoic ones is important for the understanding of the pared with the modern kerogen contents (Pinti et al., evolution of the Precambrian atmosphere (Farquhar et al., 2001), and that those of the late Archean are close to 0‰ 2000). The presence of anomalous Δ33S in Archean sam- AIR (Beaumont and Robert, 1999). However, positive ples and its absence from the beginning of the Proterozoic δ15N values similar to contemporary values have been

onwards led to the postulation that photolysis of SO2 took observed in the Paleoproterozoic sedimentary sequences place in the Archean atmosphere with very low oxygen (Beaumont and Robert, 1999). Such a shift is supposed to 192 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 193

Figure 10. Summary of evidence for reducing (bottom half) and oxidizing (upper half) conditions during the Precambrian. Note polarization of all the reducing evidence to the Archean and vice versa. be consistent with oxygen increase during the Paleopro- view emerging among various workers. The exact dating terozoic (Holland, 2002). Although the recent compilation of the initial rise in atmospheric oxygen at ~ 2.32 Ga of δ15N data of cherts and black shales indicates a similar (Bekker et al., 2004) may have a significant relation to the trend of enrichment in Proterozoic sedimentary rocks, the styles and rates of processes that might have caused the hydrothermal micas seem to show a reverse trend, i.e., oxygenation as well as to the consequences of the oxygen decreasing δ15N values from the Archean to the present (Jia rise, especially to the biological realm. It may be possible and Kerrich, 2004). In another nitrogen isotope study on that nonreducing and locally oxidizing conditions were the shales of 3.25－2.22 Ga old sequences, it has been sug- prevalent during the Archean as well (Nisbet and Sleep, gested that there is no difference between the present－day 2001), although widespread oxygenated environments nitrogen cycle and that operative since at least middle became more abundant from Proterozoic onwards. Archean onwards (Yamaguchi et al., 2002). Clearly, the beginning of the Proterozoic marks a dominant change in the Earth as a system enabling it to func- Summary on the timing of the oxygen rise tion more like the present day (Cloud, 1983).

Many lines of evidence have been presented to deduce the CAUSAL PROCESSES OF ATMOSPHERIC exact timing of the oxygen rise. The secular variations in OXYGEN RISE BIF characteristics; abundance of detrital heavy minerals, red beds and sulfates; redox－sensitive elements in shales; The primitive atmosphere contained very little or no free compositions of paleosols; and stable isotope composi- molecular oxygen and it must be inorganic and/or organic tional records of carbon, sulfur and nitrogen all suggest processes through which the presence of oxygen has been that atmospheric oxygen started increasing during the established. The photolysis of water vapor (H2O + hν → Paleoproterozoic. A summary of important evidence con- OH + H↑; 4OH → 2H2O + O2) and the photosynthetic cerning the atmospheric oxygen rise is presented in Figure splitting of the water molecule (CO2 + H2O → CH2O + 10. A polarization of evidence indicative of oxidative con- O2) are the two important processes of oxygen produc- ditions to the Proterozoic and vice versa can be regarded tion. However, the production rate of these processes has to favor the Proterozoic oxygen－rise models. However, to overwhelm the rate of oxidation of reductants present some evidence and arguments still support the view that in the crust and ocean in order to establish and maintain － the atmospheric oxygen level was high and remained con- the presence of free molecular O2 in the atmosphere stant since the early Archean. Initiation of oxygenic pho- hydrosphere system. The main reductants that must be tosynthesis as early as the late Archean (Brocks et al., oxidized are carbon, sulfur and metallic ions (chiefly Fe), 1999) favors such early oxygenation models. The MIF in generated from various sources such as mantle out－gas- S isotopes and the Fe retention pattern in paleosols, how- sing during volcanism and as byproducts of photosynthe- ever, point more towards the Proterozoic rise models. It sis, alteration, etc. The rate of the positive feedback mech- can be seen from Figure 10 that evidence indicative of anism over the negative one has in effect determined the oxygen rise started appearing as early as 2.45 Ga and pattern as well as the timing of the oxygen rise during the spanned up to 1.85 Ga. Such a spread in the timing of var- Precambrian. An early oxygenation model suggests the ious pieces of evidence can be interpreted in terms of an onset of very early photosynthesis followed by a rapid increase in oxygen level during the Paleoproterozoic—a increase in atmospheric oxygen and its subsequent stabili- 192 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 193

zation. Using a kinetic approach in which the carbon and enon. Therefore, the establishment of free molecular oxy- oxygen cycles were coupled, Lasaga and Ohmoto (2002), gen by the Proterozoic must be a result of the cumulative suggested that the dynamics and stability of atmospheric effort of gradual increases in organic carbon in the sedi-

O2 have been mainly controlled by the oxidation of or- ments. ganic carbon in the crust, the composition and flux of vol- Based on the running averages of isotopic composi-

canic gases and the level of atmospheric CO2. tions of carbonate and organic fractions, Des Marais et al. The models that propose a later (Paleoproterozoic) (1992) have proposed that the fraction of organic carbon

origin for atmospheric free molecular oxygen require buried (ƒorg) has increased from ~ 10 to 20% in the period either an increase in the sources of oxygen or a decrease between 2.6 and 2.2 Ga. This enhancement in organic car- in its sinks. The disassociation of water vapor during pho- bon burial during the period ~ 2.2－2.0 Ga has been con- tolysis and subsequent escape of hydrogen to space sidered to be affected by increased rates in tectonic pro- appears as a legitimate inorganic means through which cesses, such as rifting and orogeny (Des Marais et al., oxygen enrichment of the atmosphere might have taken 1992). Using a numerical approach coupling the carbon, place. However, the magnitude of its effect appears less strontium, sulfur and atmospheric oxygen cycles, than the sizes of reductant reservoirs to be satisfied with Godderis and Veizer (2000) proposed that the oxygen- the free oxygen generated by such reaction (Kasting and ation of the Earth’s exosphere is a consequence of conti- Donahue, 1981). Conventionally it is believed that burial nental crustal growth and therefore of tectonic evolution.

of organic carbon has played a critical role in the oxygen A rise in ƒorg during the Neoproterozoic can be envisaged rise (Holland, 1978). However new hypotheses have been from the carbon isotope excursions, which show yet proposed emphasizing the decrease in oxygen sinks as the another episode of an increase in oxygen level. This led to causal processes for atmospheric oxygen rise (Catling et the proposition of a stepwise oxygen increase pattern dur- al., 2001; Kump et al., 2001; Holland, 2002). This is ing the Proterozoic (Des Marais et al., 1992). The sulfur based on the emergence of evidence that suggests a much isotope record also seems to be consistent with such a earlier origin of oxygenic photosynthesis, by about 2.7 Ga stepwise pattern during the Proterozoic (Canfield and (Brocks et al., 1999) or even as early as 3.7 Ga (Rosing Teske, 1996). The global positive－δ13C excursions must and Frei, 2004). In the following, hypotheses regarding have resulted from the increased organic carbon burial processes being responsible for oxygen rise are briefly during the Paleoproterozoic (Karhu and Holland, 1996) as reviewed. well as the Neoproterozoic (Kaufman, 1997). This attests to the importance of the carbon biogeochemical cycle in Conventional theories of organic carbon burial the oxidation of Earth’s environment. Some positive δ13C excursions already occurred in the 2.45 Ga old carbonate It is now firmly believed that photosynthesis is the pri- sequences of the Transvaal Supergroup (Buick et al., mary oxygen producing mechanism because of its over- 1998; Bekker et al., 2001), although the major global whelming rate compared with the photolytic breakdown δ13C excursion event (2.22－2.06 Ga) postdated the initial of water. Most of the oxygen produced during photosyn- oxygenation event at 2.32 Ga (Bekker et al., 2004). These thesis (99.9%) is consumed back during the decay of dead findings suggest that the carbon cycle has indeed some organic matter and respiration, so that the photosynthetic role in the oxygen rise. It has been estimated that the reaction appears to be reversible. However, the amount of δ13C values of about 12‰ during the 2.22－2.06 Ga period

organic carbon incorporated in the sediments is propor- indicate a ƒorg of ~ 50% (Sreenivas et al., 2001b). The tionate to the amount of free molecular oxygen accumu- resultant oxygen release would be of the order of 2.0 ± 0.6 lated in the atmosphere－hydrosphere system. Broecker × 1022 g, which accounts for 12－22 times the content of (1970) first proposed that the atmospheric oxygen and oxygen in the present day atmosphere (Karhu and burial of organic carbon have attained dynamic equilib- Holland, 1996; Holland, 2002). rium since the Precambrian, based on the relative con- There are some important limitations of these mod- stancy of isotopic compositions of carbonate and organic els. The positive δ13C excursions prior to the initial oxy- carbon during the Phanerozoic (Keith and Weber, 1964). gen presence at 2.32 Ga seem highly local in nature and, Such an isotopic constancy suggests that the fraction of therefore, the oxygen rise appears to be followed by the organic carbon buried remained constant throughout geo- carbon cycle disturbance. The carbon isotopic ratios of logical history. Based on similar isotopic constancy carbonate and organic fractions remained constant almost

throughout the Precambrian, Schidlowski et al. (1975) from 3.5 Ga onwards, which indicates that the ƒorg proposed that the equilibrium between organic carbon and (~ 20%) remained constant (Schidlowski, 1988). Hence, atmospheric oxygen is a much earlier (3.85 Ga) phenom- the oxygen production should be similar to the present 194 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 195 day (Ohmoto, 1997). The running averages of carbon iso- initiated around 2.7 Ga seems to have culminated in oxi- tope compositions for 0.1 Ga (Des Marais et al., 1992) dation of the entire mantle by about 2.5 to 2.4 Ga. This may result in erroneous ƒorg values, considering the effects must have resulted in a decrease of reducing fluxes asso- of methanotrophs on the isotopic compositions of carbon- ciated with volcanic activity during the Archean－ ate rocks aged 2.6－2.7 Ga. Some models of crustal evolu- Proterozoic transition, enabling enrichment of free molec- tion suggest that the volume of the crust remained con- ular oxygen in the atmosphere (Kump et al., 2001; Sleep, stant right from the early Archean (e.g., Green et al., 2001). This hypothesis explains the mechanism through 2000). Hence, the growth of organic carbon reservoir in which oxidation of the mantle has been established and its the crust with time seems to be unlikely. Another impor- role in oxidizing the exosphere. However, these models tant objection to the decoupling of carbon burial and oxy- require evidence to establish that the mantle ƒO2 values genation is the necessity for the buried organic carbon to have changed with time. The evidence, in the form of be subducted irreversibly. Failing this condition can lead variations in the V/Cr ratios of basalts, indicates that the to consumption of the oxygen by the organic carbon, ƒO2 values of the Archean and present day magmas are through either metamorphism or re－exposure in the long－ within 0.5 log units (Canil, 1997; Canil, 1999; Delano, term geological cycle (Catling et al., 2001). Despite these 2001). Subsequently, it has been argued that even such a 13 constraints, we have seen the coincidence of positive δ C small difference, of 0.5 log units in ƒO2, is sufficient to excursions and several pieces of evidence for the oxygen cause the transition in mantle fluxes that has affected the rise during the Paleoproterozoic as well as the Neoprote- oxygen rise (Holland, 2002). In addition, the V/Cr ratios rozoic. Further examination of the role of the carbon cycle of Archean komatiites may represent the magmatic ƒO2 but in the oxygen evolution during the Precambrian is still not that of the mantle (Canil, 1997). These discussions required. make mantle oxidation a viable mechanism (Li and Lee, 2004) for explaining the initial oxygen rise. However, in a Secular variations in mantle fluxes more recent study employing V/Sc ratios, which are thought to be more robust and representative of mantle

Secular cooling of mantle would have resulted in the conditions than V/Cr, it has been shown that the ƒO2 of the dwindling of reducing fluxes from volcanism with time mantle has remained constant at least since the early and, hence, it may be possible to attribute the oxygen rise Archean (Li and Lee, 2004). In summary, the evidence in the Paleoproterozoic period to this gradual change in from redox－sensitive indicators in the Archean to pres- Earth history (Holland, 2002). However, this seems ent－day basalts, are not consistent with each other. Hence, unlikely as increased volcanic fluxes during the early his- it is not clear whether the accumulation of free molecular tory would have implied higher CO2 fluxes as well. oxygen in the atmosphere during the Paleoproterozoic is

Considering a constant ƒorg value from 3.5 Ga onwards, related to major or minor changes in the oxidation state of such enhanced CO2 fluxes would have resulted in higher the mantle. organic carbon burial and therefore a much earlier oxygen rise. Recognizing this conundrum, Kasting et al. (1993) Biogenic methane and hydrogen escape proposed that there has been a gradual shift in the composition of volcanic fluxes from reducing to oxidizing by the All the buried organic carbon should be irreversibly sub- end of Archean, which caused the increase of atmospheric ducted in order to have a net effect on the oxygen increase oxygen. Kasting et al. (1993) suggested that such a pro- in the atmosphere (Catling et al., 2001). Therefore, alter- gressive change in reducing volcanic fluxes could be native processes have been proposed to maintain the accomplished by a progressive loss of hydrogen to space, increase in oxygen; for example, organic carbon is con- which might have resulted in an increase of the overall verted to methane biogeochemically and then hydrogen is oxidation state of the Earth and thereby also the mantle. lost from the methane photochemically in atmosphere Expanding these lines of argument, it has been further (Catling et al., 2001). The biogenic methane under UV shown that a decrease in the average oxygen fugacity radiation breaks down to carbon and hydrogen in the

(ƒO2) of volcanic gases by 2 log units from that of the upper atmosphere leading to escape of hydrogen into present is sufficient to maintain a reducing mantle (Kump space. The overall chemistry of such a reaction, CO2 + et al., 2001). It has been argued that oxidation of Fe and H2O → CH4 + 2O2 → CO2 + O2 + 2H2 (↑ space), would its subsequent incorporation into the mantle along with have affected a net increase in the oxygen content (Catling sediments might have led to an overall increase in the oxi- et al., 2001). This mechanism explains the missing reser- dation state of the lower mantle (Kump et al., 2001). voir of organic carbon in the 2.22－2.06 Ga sequences Overturn of such a lower mantle during the plume events (Melezhik and Fallick, 1996), as the organic carbon 194 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 195

would have been converted to methane in the presence of of crustal oxidation states to support the methane－hydro- methanogens during organically mediated diagenesis. gen escape hypothesis (Kasting, 2001). The methane－rich According to this model, the Precambrian methane－rich Archean atmosphere models have mainly cited the atmosphere is a prerequisite to be effective in oxygenat- absence of siderite in late Archean and Paleoproterozoic

ing the environment. The antiquity of methanogenic bac- paleosols as strong evidence for low atmospheric PCO2 (Rye teria to late Archean times is well established (Hayes, et al., 1995). However, in a recent experimental study on － −5 1994; Dix et al., 1995; Rye and Holland, 2000b). The biotite dissolution under oxygen deficient (PO2 < 3 × 10 － absence of siderite in Precambrian paleosols has been atm) and CO2 rich (PCO2 1 atm) conditions, Murakami et considered to indicate that methane played a more impor- al. (2004a) have found that vermiculite is the secondary

tant role as a greenhouse gas than did CO2 during the product rather than siderite. This experimental result Precambrian (Rye et al., 1995). Hence, the role of hydro- shows that the absence of siderite in Archean paleosols

gen escape from methane breakdown would have been may not point at low PCO2 and thereby high PCH4 condi- very effective during the Precambrian in accomplishing tions. Further, on the basis of the carbon isotope composi- oxygen rise. Photochemical models also suggest high tion of siderites in BIFs, Ohmoto et al. (2004) recently

methane contents in the Precambrian atmosphere (Pavlov suggested that CO2 is the important greenhouse constitu-

et al., 2000). Another important observation, which sup- ent, rather than CH4. Importantly, if methane had a critical ports the role of methane and hydrogen in oxygenating role both as a greenhouse constituent and in oxidizing the the atmosphere, came from the observations that the mod- environment, then the initiation of glacial cycles and the

ern cyanobacterial mats on coastal mudflats release 2 H , oxygen rise should be coeval during the Proterozoic. 33 CO and, more importantly, CH4 during nighttime, i.e., However, the evidence in the form of Δ S record and gla- under low oxygen conditions (Hoehler et al., 2001). If the cial deposits from the Transvaal Supergroup indicate that ancient organism also mimicked this mechanism, it would global cooling during the Paleoproterozoic perhaps pre- obviously have a profound influence on oxygen release. dated the oxygen rise. The biogenic methane and hydrogen escape hypoth- High atmospheric methane concentrations have also esis further proposes that the free molecular oxygen left been advocated for the entire Proterozoic period despite over has been mainly utilized by the reductant reservoirs their short－lived nature in oxygenated atmosphere (Pavlov of the crust, which eliminates the secular changes in man- et al., 2003). It has been argued that the high atmospheric tle oxidation states from the scenario of oxygen evolution methane concentrations can be possible under higher (Catling et al., 2001). The oxidation of the crust resulted input fluxes than the present day during methanogenesis. in decreased amounts of reducing gases released by low－ However, Kaufman and Xiao (2003), using an ion micro- temperature metamorphic processes. Initial oxygen rise is probe, recently reported carbon isotope compositions of － assumed to be a rapid process, being established as soon individual acritarchs and estimated a PCO2 of 10 200 PAL.

as the net photosynthetic production exceeded the input of These CO2 concentrations seem to be sufficient to over- reduced gases (Catling et al., 2001). Kasting (2001) fur- come the decreased solar luminosity as predicted by the ther proposed that the oxidation of the crust by the one－dimensional climate model (Kasting, 1987, 1993). Paleoproterozoic may have been accomplished by either This study clearly emphasizes the need for improved cali-

oxidation during sea floor alteration, similar to present bration of past CO2 levels before attributing methane as day serpentinization, or the oxidation of Fe associated the dominant greenhouse constituent as well as the reason with BIF deposition. for oxygen rise. It may be pointed out here that much

Despite these apparently convincing arguments, sev- higher CO2 concentrations have been inferred at ~ 3.2 Ga, eral questions still remain regarding the role of biogenic which is consistent with theoretical models based on the methane and hydrogen escape on oxygen release. Wide- presence of Fe carbonate in river gravels from South spread methanogenesis is essential to maintain a high Africa (Hessler et al., 2004). methane atmosphere during the entire Archean, which would have produced a wide－range of δ13C values in the Summary on the causal processes carbonates, e.g., those of the ~ 2.7 Ga old Crixas greenstone belt (Dix et al., 1995). However, such large varia- Several mechanisms have been invoked as the causal pro- tions are uncommon in the Archean and Paleoproterozoic cess or processes of oxygenation of the Earth’s atmo- carbonate record. Although the reported evidence for sphere. The central issue is a better comprehension of the methanogenesis is as old as 2.7 Ga, a much older origin quantitative aspects of the evolution of atmospheric oxy- for methanotrophs cannot be precluded. There is a lack of gen, which will definitely place better constraints on the both qualitative and quantitative indicators of the change causal processes. Holland (2002) attributed the oxygen- 196 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 197 ation to the role of dwindling reductant fluxes in volcanic that the availability of oxygen as an energy source trig- gases. Biogenic methane and hydrogen escape—a neg- gered the evolution of complex life (Hedges et al., 2004). lected biogeochemical mechanism—has also been envis- The appearance of megascopic eukaryotes by ~ 2.1 Ga aged as a possible mechanism of the oxygen enrichment may further verify the above supposition (Han and process (Catling et al., 2001). It may be difficult to pro- Runnegar, 1992). The appearance of Ediacaran fauna at vide evidence for some of the above arguments, e.g., the Precambrian－Cambrian boundary is coeval with yet methane and hydrogen escape. For others, such as mantle another oxygenation event during the Neoproterozoic. oxidation, the evidence may not be compelling. The This may deeply implicate the entwined nature of envi- enveloping nature of positive δ13C excursions with the ronment and life on the Earth (Fig. 11; Lenton et al., evidence indicating the presence of free molecular oxy- 2004). It has been proposed that microorganisms are gen contrasts with such scenarios, upholding the conven- equally responsible for changes in the composition of tional wisdom in understanding oxygen evolution during atmosphere, truly attesting the coevolutionary nature of the Archean－Proterozoic transition. the Earth’s surface (Kasting and Siefert, 2002). The lack of dissolved oxygen in deep oceans for a prolonged CONSEQUENCES OF ATMOSPHERIC period between 1.8 and 0.8 Ga has been assumed to be a OXYGENATION significant factor in the mid－Proterozoic algal evolution (Anbar and Knoll, 2002). According to Kirschvink et al. The oxygen rise has affected some irreversible changes in (2000), the oxygenation event might have triggered a the course of the history of the Earth, especially in the compensatory evolutionary branching in the Fe/Mn super- biological realm. Oxygenation led to the biological inno- oxide dismutase enzyme. It appears that the oxygen levels vation of aerobic, complex, multicellular life laying foun- have constrained the rate of biological evolution both dations for the current status of the surface. Recent efforts qualitatively and quantitatively (Knoll, 2003). to create a new timeline for eukaryote evolution using the The prolonged reducing conditions during the molecular dating technique indicates significant relation- Archean period encouraged BIF deposition. It is well ships between the complexity of life forms and the known that Fe oxides can efficiently adsorb phosphate on increase in oxygen levels (Hedges et al., 2004). It has to their surfaces. Based on this, the phosphate concentra- been further concluded that mitochondria and multicellu- tion in the seawater during the Precambrian has been esti- lar organisms started appearing at ~ 2.3 Ga, soon after the mated using BIF compositions (Bjerrum and Canfield, initial oxygen rise. Enhancement in eukaryotic complex- 2002). It has been suggested that BIFs during the Archean ity at ~ 1.5 Ga has been attributed to the appearance of have acted as a major sink for phosphate, thus lowering plastids that can generate oxygen. This clearly indicates its concentration and affecting a nutrient limitation on

Figure 11. The entwined nature of atmospheric oxygen and the biosphere at the surface of Earth. The oxygen increase seems to have affected major changes in the course of biological evolution. It may be no- ticed that megascopic eukaryotes started to appear at ~ 2.1 Ga (Han and Runnegar, 1992), soon after the increase in atmospheric oxygen. Also, the radiation of macroscopic animal fauna during the Neoproterozoic may have resulted from yet another episode of increase in atmospheric oxygen. However, triploblastic animals might have originated much earlier, by ~ 1.5 Ga (Seilacher et al., 1998; Rasmussen et al., 2002). The origin of plastids, which have helped the eukaryotes to produce their own oxygen, seems to have affected more diverse forms of life (Hedges et al., 2004). 196 B. Sreenivas and T. Murakami Emerging views on the evolution of atmospheric oxygen during the Precambrian 197

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