COMMENTARY

An early productive ocean unfit for aerobics

Timothy W. Lyons1 and Christopher T. Reinhard Department of Earth Sciences, University of California, Riverside, CA 92521

rasping the big picture of the banded iron formations (BIFs)—the early ocean used to be easy: no smoking gun for the earlier ferruginous , and then oxygen. The ocean. In other words, Canfield (1) ar- crux of that popular model gued that H2S began to build up Ghinged on the almost universally accepted throughout much, if not all, of the deep , or GOE, during ocean beginning Ϸ1.8 billion years ago which appreciable free oxygen (O2) first and persisted ubiquitously for a billion accumulated in the atmosphere about 2.4 or more years. billion years ago. At the same time, as the The is nothing short old argument goes, the O2-free, iron-rich of paradigm-busting, and evidence for earlier ocean gave way to one with oxygen euxinic (anoxic and sulfidic) conditions at all depths. About a decade ago, in the Proterozoic ocean has emerged Canfield (1) offered a very different over the past decade (refs. 3–7, re- possibility—that ventilation of the deep viewed in ref. 8). In fact, confidence in ocean lagged behind the GOE by more this model has inspired a new genera- than a billion years, resulting in a vast, tion of research exploring the potential deep reservoir of , but biological implications of global euxinia, long-held presumptions about photosyn- such as decreased availability of bioes- thetic life in the surface waters remained sential trace metals (9). Molybdenum untouched. In the first comprehensive and copper, for example, are less solu- biogeochemical model of this ‘‘Canfield ble in the presence of H2S and play key Ocean,’’ Johnston et al. (2) in a recent enzymatic roles in the nitrogen cycle, issue of PNAS present a stunningly including N2 fixation by cyanobacteria different take on those early (7, 9, 10). photosynthesizers—one in which the up- Enter Johnston et al. (2). Astutely, per, light-containing layers indeed drove the authors recognized that a challenge biological production but without the ex- Fig. 1. A modern analog for the ancient sulfidic ocean? (Upper) Mahoney Lake, British Columbia, to the Canfield model is maintaining pected concomitant release of oxygen. Canada—perhaps like the Proterozoic ocean (2)— oxygen deficiency over such a long pe- And it is this feedback that may explain a contains abundant H2S in the . In the riod. The problem: a tiny but critically troubling uncertainty about the Canfield case of Mahoney Lake, the O2–H2S interface is only important percentage of sinking biomass Ocean and this time interval in general— 7 m deep—ideal conditions for anoxygenic photo- escapes decay in the deep ocean and exactly how oxygen in the biosphere re- synthesis. (Lower) A ‘‘plate’’ of profuse purple, underlying and is buried, typi- mained at only a fraction of modern levels S-oxidizing, anaerobic bacteria at this interface cally yielding a net increase in atmo- generates more than half of the primary produc- for so long after the GOE. spheric and seawater O2. And a strong Populations of photosynthesizing phy- tion in the lake. (Lower photo by J. Glass, Arizona State University, Tempe, AZ.) negative feedback is in place because toplankton abound in the sunlit portions the anoxia induced by organic degrada- of the modern surface ocean, often to tion actually increases the fraction of depths of 100 m or more. Using energy were still only a fraction of today’s, Can- organic matter that escapes decay. from the sun, they represent the domi- field could confidently infer similarly As is often the case, old rocks make nant pathway by which carbon dioxide is lower concentrations in the ocean, given more sense when viewed through a lens fixed in the ocean and are the founda- the exchange between the two. Add in focused on the modern ocean. After hav- tion (the primary producers) of the food the O consumption facilitated by a bio- ing such a look, Johnston et al. (2) asked chain. And O is their famous waste 2 2 logical pump assumed to be robust, and a key question: what if the primary pro- product. Much of the biomass formed in duction in the surface ocean that settles the surface ocean is degraded by aerobic anoxic conditions may have been perva- and decays to facilitate O2 loss in the bacteria on the spot, consuming the oxy- sive throughout the deep global ocean. Although O remained low or absent deep ocean was triggered by a photosyn- gen at a rate almost as fast as the gas is 2 thetic pathway that does not produce oxy- produced. The rest settles to the deep in the deep ocean, post-GOE levels in the atmosphere were sufficiently high (it gen? Today, we only have to look to the ocean, where the O2-consuming respira- doesn’t take much) to oxidize the min- and many stratified lakes to see tion continues. This shallow-to-deep that such anoxygenic does eral (FeS2) during on flow of material is known as the 2Ϫ occur and can even dominate primary the continents, leading to (SO ) . 4 production, at least in lakes. delivery to the ocean by rivers. This new Canfield (1) speculated on how an There are two key ingredients to such flux of sulfate is key to the story be- analogous biological pump and associ- systems. First, the subsurface waters in ated oxygen loss in the deep ocean cause as it accumulated in the still might have operated in the early world, anoxic deep ocean, sulfate-loving, O2- after the GOE but well before the rise loathing bacteria rereduced the sulfur to Author contributions: T.W.L. and C.T.R. wrote the paper. of animals about 700 million years hydrogen sulfide (H2S), driving the solu- The authors declare no conflict of interest. ago—during a time interval known as bility of dissolved iron in seawater to See companion article on page 16925 in issue 40 of volume the Proterozoic. There are two key near null levels through pyrite formation 106. pieces in this puzzle. First, because O2 rather than iron oxidation. This loss of 1To whom correspondence should be addressed. E-mail: levels in the atmosphere, in general, iron dealt a deathblow to the vast [email protected].

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0910345106 PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 ͉ 18045–18046 Downloaded by guest on September 24, 2021 the lake or ocean need to be anoxic and authors’ ‘‘gauntlet.’’ Specifically, tions (6). And there are challenges to rich in dissolved H2S—so far so good they argue, upward returning N is con- maintaining H2S in near-surface waters for the Canfield Ocean. Second, those sumed in the deep part of the photic in a wind-stirred open ocean beneath an euxinic waters need to extend upward zone by the anoxygenic phototrophs and O2-containing atmosphere. into the photic zone, within the penetra- by processes that convert bioavailable Another important issue is whether ϩ tive reach of sunlight. Certainty of shal- (‘‘fixed’’) nitrogen (e.g., NH4 )toless global rates of biological nitrogen fixa- low euxinia is a tougher box to check available N2 under oxygen-deficient con- tion would have been able to fuel the for the Proterozoic. More on this below, ditions. Possible outcomes are ecological export flux of organic matter out of the but for now, let’s have look through that dominance by organisms that can pro- photic zone necessary to maintain eu- modern lens. vide their own bioavailable N (diazo- xinia on long timescales. Loss of fixed N The Black Sea is Ϸ2,000 m deep, and, trophs, such as cyanobacteria) at the under anoxic conditions, combined with as the largest euxinic basin on the modern expense of eukaryotic algae and, impor- global limitation of N2 fixation owing to Earth, all but its upper 100 m are anoxic tantly, a decline in the relative amount trace metal deficiencies (7, 9), could and loaded with H2S. Despite being at the of oxygenic photosynthesis. have acted as a negative feedback lower limits of adequate light penetration, Whether right in every detail or not, against euxinia, thereby decreasing the this interface supports some primary pro- Johnston et al. (2) have designed a far- level of anoxygenic production. Happily, duction of organic matter by green sulfur reaching thought experiment loaded this novel view of ecology in the ocean bacteria. These phototrophic anaerobes with roadmaps for future research. comes with predictions, testable, for ex- are sustained by the juxtaposition of H2S, Among the remaining questions: how ample, through analysis of diagnostic which they oxidize for energy, and light, strong is the physical evidence for a organic biomarkers (molecular finger- which catalyzes that oxidation. Euxinia, Canfield Ocean—the root of the prints) and their isotopic properties. To and shallow euxinia in particular, is not a Johnston et al. model? There is cer- date, direct evidence for voluminous common condition in the modern ocean; tainly evidence that euxinia was wide- production by cyanobacteria and/or an- the other best examples come from lakes, spread during the Proterozoic, likely aerobic S-oxidizing bacteria has not where purple S-oxidizing anaerobic bacte- much more so than today, but few if any been found. ria also thrive, presumably when H Sis of the data actually demand a global 2 At a minimum, Johnston et al. (2) especially shallow (Fig. 1). Adding to the Black Sea. have produced the first comprehensive mix, Johnston et al. (2) point out that cya- Johnston et al. (2) suggest that eu- conceptual model for chemical cycling nobacteria, well-known perpetrators of xinia may have been confined to mid- and life in the ocean during the Protero- oxygenic photosynthesis and the organism depths in the water column, much like credited with the first oxygenation of the the oxygen minimum zones seen widely zoic, with talking points galore awaiting atmosphere, can switch to anoxygenic in the modern ocean. In such a case, dissection in graduate seminars. If that photosynthesis under euxinic conditions the deep ocean may have been O - is not enough for fans of the early 2 Earth, the authors even extrapolate their and subsist on H2S. containing, or ferruginous, or sulfidic; it As in any whodunit, Johnston et al. is hard to know—that record has largely arguments to speculate on the causes (2) introduce a lot of characters and been lost through subduction of deep behind Earth’s animal-favoring, second subplots along the way. Amidst the de- ocean crust. Very limited data suggest great step in atmospheric oxygenation tails, however, a simple, elegant story that at least weakly oxygenated deep late in the Proterozoic. A return to iron- line binds the pieces: a Proterozoic sea conditions were possible (7, 11). Also, dominated conditions in the deep ocean, after a billion years of efficient pyrite rich with H2S in the photic zone could most of the available records, with the have sustained vast key exception of molybdenum isotopes, burial under euxinia (12), may have without concomitant generation of oxy- are of proxies that speak mostly to local seeded the demise of their anoxygenic gen. The ocean gains a sink for O2 via conditions, and restricted basins analo- factory, thriving up to that point on the decay of this biomass without the gous to the modern Black Sea, not eas- H2S. There are more than a few layers offsetting source. ily subducted, may be skewing our of conjecture stacked at this point in the Because the biological pump shuttles interpretations of the ancient global story, and the possibility that analogous, organic matter to the deep ocean, the ocean. The extent of euxinic bottom wa- iron-based pathways of anoxygenic pho- surface waters show the wear of their ters as constrained by the molybdenum tosynthesis may have taken over remains losses through deficiencies in nitrogen isotopes need not have been anything fodder for conjecture. But if Johnston et and phosphorus, among other key nutri- close to global. An even greater chal- al. are right, the torch of the dominant ents. It is primarily through the up- lenge is convincing the community that primary producers may have been welling of deep waters and the Proterozoic euxinia was widespread and passed, for the first time, to O2-yielding they contain from organic decay that shallow. There is precious little evidence photosynthesis, and the atmosphere and primary production can persist. This re- for H2S within the early photic zone; ocean would never again look so persis- lationship is the underpinning of the what does exist may reflect local condi- tently and pervasively oxygen lean.

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