Considerable discussion surrounds the potential role of anoxygenic phototrophic Fe(II)-oxidizing bacteria in both the genesis of Banded Iron Formations (BIFs) and early marine productivity. However, anoxygenic phototrophs have yet to be identified in modern environments with comparable chemistry and physical structure to the ancient Fe(II)-rich (ferruginous) oceans from which BIFs deposited. Lake Matano, Indonesia, the eighth deepest lake in the world, is such an environment. Here, sulfate is scarce (<20 mol⅐liter ؊1 ), and it is completely removed by sulfate reduction within the deep, Fe(II)-rich chemocline. The sulfide produced is efficiently scavenged by the formation and precipitation of FeS, thereby maintaining very low sulfide concentrations within the chemocline and the deep ferruginous bottom waters. Low productivity in the surface water allows sunlight to penetrate to the >100-m-deep chemocline. Within this sulfide-poor, Fe(II)-rich, illuminated chemocline, we find a populous assemblage of anoxygenic phototrophic green sulfur bacteria (GSB). These GSB represent a large component of the Lake Matano phototrophic community, and bacteriochlorophyll e, a pigment produced by low-light-adapted GSB, is nearly as abundant as chlorophyll a in the lake's euphotic surface waters. The dearth of sulfide in the chemocline requires that the GSB are sustained by phototrophic oxidation of Fe(II), which is in abundant supply. By analogy, we propose that similar microbial communities, including populations of sulfate reducers and photoferrotrophic GSB, likely populated the chemoclines of ancient ferruginous oceans, driving the genesis of BIFs and fueling early marine productivity.anoxygenic photosynthesis ͉ banded iron formation ͉ green sulfur bacteria ͉ iron oxidation ͉ Lake Matano
Dissecting ancient microbial sulfur cycling Before the rise of oxygen, life on Earth depended on the marine sulfur cycle. The fractionation of different sulfur isotopes provides clues to which biogeochemical cycles were active long ago (see the Perspective by Ueno). Zhelezinskaia et al. found negative isotope anomalies in Archean rocks from Brazil and posit that metabolic fluxes from sulfate-reducing microorganisms influenced the global sulfur cycle, including sulfur in the atmosphere. In contrast, Paris et al. found positive isotope anomalies in Archean sediments from South Africa, implying that the marine sulfate pool was more disconnected from atmospheric sulfur. As an analog for the Archean ocean, Crowe et al. measured sulfur isotope signatures in modern Lake Matano, Indonesia, and suggest that low seawater sulfate concentrations restricted early microbial activity. Science , this issue p. 703 , p. 742 , p. 739 ; see also p. 735
We examined the chemical composition of the water column of Lake Matano, Sulawesi Island, Indonesia, to document how the high abundances of Fe (hydr)oxides in tropical soils and minimal seasonal temperature variability affect biogeochemical cycling in lakes. Lake Matano exhibits weak thermal stratification, yet a persistent pycnocline separates an oxic epilimnion from anoxic meta-and hypolimnions. The concentration of soluble P in the epilimnetic waters is very low and can be attributed to scavenging by Fe (hydr)oxides. Chromium concentrations in the epilimnion are high (up to 180 nmol L 21 ), but below U.S. Environmental Protection Agency guidelines for aquatic ecosystems. The concentration of chromium decreases sharply across the oxic-anoxic boundary, revealing that the hypolimnion is a sink for Cr. Flux calculations using a one-dimensional transportreaction model for the water column fail to satisfy mass balance requirements and indicate that sediment transport and diagenesis play an important role in the exchange of Fe, Mn, P, and Cr between the epilimnion and hypolimnion. Exchange of water between the epilimnion and hypolimnion is slow and on a time scale similar to temperate meromictic lakes. This limits recycling of P and N to the epilimnion and removal of Cr to the hypolimnion, both of which likely restrict primary production in the epilimnion. Owing to the slow exchange, steep concentration gradients in Fe and Mn species develop in the metalimnion. These concentration gradients are AcknowledgmentsWe thank the International Nickel Company (INCO) Canada and PT INCO Tbk. for their financial and logistical support of both field and laboratory work. Support for Sean A. Crowe was partly provided by a Natural Sciences and Engineering Research Council (NSERC) Industrial Partnership Scholarship sponsored by INCO Canada. We are grateful to Bill Napier, Les Huelett, and Matt Orr for logistical support; Jim Gowans for the use of his patio boat, the
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