S CIENCE’ S C OMPASS ● REVIEW REVIEW: GEOCHEMISTRY Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge? A. D. Anbar1* and A. H. Knoll2 contrast, weathering under a moderately oxidiz- Recent data imply that for much of the Proterozoic Eon (2500 to 543 million years ing mid-Proterozoic atmosphere would have 2– ago), Earth’s oceans were moderately oxic at the surface and sulfidic at depth. Under enhanced the delivery of SO4 to the anoxic these conditions, biologically important trace metals would have been scarce in most depths. Assuming biologically productive marine environments, potentially restricting the nitrogen cycle, affecting primary oceans, the result would have been higher H2S productivity, and limiting the ecological distribution of eukaryotic algae. Oceanic concentrations during this period than either redox conditions and their bioinorganic consequences may thus help to explain before or since (8). observed patterns of Proterozoic evolution. Is there any evidence for such a world? Canfield and his colleagues have developed an argument based on the S isotopic compo- n the present-day Earth, O2 is abun- es and forms insoluble Fe-oxyhydroxides, sition of biogenic sedimentary sulfides, 2– dant from the upper atmosphere to thus removing Fe and precluding BIF forma- which reflect SO4 availability and redox the bottoms of ocean basins. When tion. This reading of the stratigraphic record conditions at their time of formation (16–18). O 2– life began, however, O2 was at best a trace made sense because independent geochemi- When the availability of SO4 is strongly 2– Ͻϳ constituent of the surface environment. The cal evidence indicates that the partial pressure limited (SO4 concentration 1 mM, ϳ intervening history of ocean redox has been of atmospheric oxygen (PO2) rose substan- 4% of that in present-day seawater), H2S interpreted in terms of two long-lasting tially about 2400 to 2000 Ma (4–7). produced by BSR is depleted in 34SbyϳϽ5 2– steady states: anoxic oceans (or nearly so) Because the solubility of Fe-sulfides is per mil (‰) relative to dissolved SO4 . Frac- that persisted for some 2000 million years, also low, however, the disappearance of BIF tionation increases to as much as ϳ45‰ 2– followed by essentially modern oceans of can alternatively be taken to indicate that the when SO4 is more freely available. Larger comparable duration. Here, we review re- deep oceans became sulfidic, rather than fractionations (45 to 70‰) appear to require a cent evidence pointing to the presence of oxic, after 1800 Ma. According to this sce- cyclical process in which 34S-depleted sul- “intermediate” oceans—oxic at the surface nario, recently advanced by Canfield (8), fides are reoxidized to elemental sulfur (S0), but anoxic and sulfidic at depth—that may deep sea water became more reducing rather followed by bacterial disproportionation of 0 34 have persisted for more than 1000 million than more oxidizing at this time despite the S to produce extremely S-depleted H2S years, originating some time after ϳ1800 rise in atmospheric oxygen. Ocean anoxia (19, 20). Hence, S isotope fractionation million years ago (Ma). Aspects of the might have persisted into the Neoproterozoic Ͼϳ45‰ between sedimentary sulfides and evolutionary pattern recorded by fossils of (9), when C and S isotopic data indicate sulfates may indicate increased oxygenation Proterozoic eukaryotes may be explained another increase in the oxidation state of of the environment (21). by the scarcity of biologically essential Earth surface environments (10–13). Several changes in S isotope systematics trace metals in such sulfidic seas, suggest- At first blush, sulfidic oceans appear coun- are seen in the Precambrian geological record ing a bioinorganic bridge between environ- terintuitive in the face of contemporaneous at- (Fig. 1B) (22). BSR appears to have been in mental and biological evolution. mospheric oxygenation. However, simple mod- place by at least ϳ3470 Ma, as suggested by eling of ocean redox suggests that deep waters a fractionation of up to 21‰ (mean ϳ11‰) Sulfidic Deep Oceans would have remained anoxic if PO2 had been between S in evaporitic barite deposits and The classical argument that the deep oceans Ͻ0.07 atm and if biological productivity, which sulfide inclusions found within these sedi- became oxidized at ϳ1800 Ma is based prin- delivers reduced C to the deep sea, was at all ments (23). However, in rocks older than cipally on the disappearance of banded iron comparable to that of modern oceans (8). It is 2400 Ma, ⌬34S (the difference in ␦34S be- formations (BIFs; Fig. 1A). BIFs are mas- likely that PO2 did not approach modern values tween marine sulfate minerals—which record ␦34 2– sive, laterally extensive and globally distrib- until the Neoproterozoic (14, 15). Sulfidization S of seawater SO4 —and co-occurring uted chemical sediment deposits that consist follows from the fact that the concentration of sulfides) is typically ϽϽ20‰. From this time ⌬34 ϳ primarily of Fe-bearing minerals and silica. hydrogen sulfide (H2S) in seawater is affected until 800 to 600 Ma, S reaches 40‰, Their formation seems to require anoxic deep by the supply of both organic C and sulfate near the maximum associated with BSR, but 2– waters to deliver hydrothermally derived (SO4 )—which constitute a source of H2S rarely exceeds this value. Only in later Neo- Fe2ϩ to locations where deposition took when their reaction is catalyzed by dissimilato- proterozoic and Phanerozoic rocks does ⌬34S place [e.g., (1–3)]. Oxygenation of the oceans ry bacterial sulfate reduction (BSR)—and by approach the modern maximum of ϳ65‰. 3ϩ would produce Fe , which readily hydrolyz- the availability of O2, which acts as a reactive The biogeochemical record of S is thus con- 2– sink for H2S and inhibits BSR. Today, perva- sistent with SO4 -poor Archean oceans giving 2– sive O2 limits H2S concentrations, as has gen- way to modest SO4 concentrations, and con- 1Department of Earth and Environmental Sciences erally been the case for the Phanerozoic Eon. In sequent global enhancement of BSR, in the and Department of Chemistry, University of Roches- the Archean and early Paleoproterozoic, the Paleoproterozoic. Presumably, the rise of a ter, Rochester, NY 14627, USA. 2Department of Or- ganismic and Evolutionary Biology, Harvard Universi- low solubility of reduced S minerals in igneous moderately oxidizing atmosphere facilitated, ty, Cambridge, MA 02138, USA. and sedimentary rocks during weathering under for the first time, the delivery of large quantities 2– 2– *To whom correspondence should be addressed. E- a nearly anoxic atmosphere limited the SO4 of SO4 to the oceans (8, 24). The observation ⌬34 Ͻ mail: [email protected] supply, keeping H2S concentrations low. In that S 45‰ during the mid-Proterozoic www.sciencemag.org SCIENCE VOL 29716 AUGUST 2002 1137 S CIENCE’ S C OMPASS suggests that the oceans were oxygenated only Proterozoic basin, as might be expected in a gan to rise at this time, but the observed 2– to shallow depths during this time, and that low-SO4 ocean (32, 33). isotopic variability, not seen in Phanerozoic more extensive oxygenation did not occur until Gypsum and anhydrite (CaSO4 minerals) sulfate minerals (35), again suggests a small- 2– late in the eon (12). are common in rocks that formed along the er mid-Proterozoic global ocean SO4 reser- ϳ 2– If sulfidic conditions were common margins of 1200-Ma carbonate platforms in voir. Seawater SO4 may have remained through much of the Proterozoic Eon, inde- the Bylot Supergroup, North America, but are well below present-day levels until the end of pendent geochemical redox indicators should scarce in older rocks. ␦34S in these minerals the Proterozoic Eon (36). provide evidence of anoxia. In addition, sea- varies by up to 10‰ over 300 m of section As yet, detailed stratigraphic analyses are 2– water SO4 concentrations in the Proterozo- (34). The appearance of extensive CaSO4 too few to demonstrate unequivocally the 2– ic, although greatly elevated over Archean deposits indicates that SO4 inventories be- global nature of sulfidic deep waters in mid- values, should have been lower Proterozoic oceans. However, than at present; this prediction available data point to globally Time before present (Ma) 2– can be tested by looking for “res- extensive BSR in low-SO4 ervoir” effects in pyrite ␦34S oceans, ocean oxygenation insuf- 0 within individual sedimentary ba- 3000 2500 2000 1500 1000 543 ficient to support S dispropor- sins (25). tionation, and sulfidic bottom wa- Both predictions are met in Archean Proterozoic Eon ters in at least some marine basins Eon superbly preserved black shales Paleo- Meso- Neo- during this time. We must there- deposited ϳ1730 and 1640 Ma fore take seriously the proposition during maximum flooding of the A that the deep oceans were persis- Tawallah and McArthur basins, tently sulfidic for much of our respectively, in northern Austra- planet’s middle age. lia. Two geochemical indicators reliably differentiate sediments B Biology of Mid-Proterozoic formed beneath oxic and sulfidic 0 Oceans waters in the Black Sea (26–28) What was biology like in mid-Pro- and in Mesozoic marine basins ) terozoic oceans? Hints come from (29). The ratio of “highly reac- ‰ C isotopes and fossils, which show S ( tive” Fe (Fe present in pyrite or 34 distinctive stratigraphic trends that oxides/hydroxides) to total Fe ∆ correlate broadly with the inferred tends to be higher in sediments redox history. deposited beneath sulfidic waters * –60 Secular variation of C isotopes than in sediments deposited be- C in marine carbonates (␦13C ) +12 carb neath an oxic water column. Sim- reflects changes in the ratio of ilarly, the “degree of pyritization” organic to inorganic C removed (the proportion of reactive Fe in- from the oceans during burial in ) corporated into pyrite) tends to be ‰ sediments (37).