Arne Sturm

Photoferrotrophs thrive in an Archean Ocean analogue

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 μmol·liter−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 lakes 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.

The methane cycle in ferruginous Lake Matano

In Lake Matano, Indonesia, the worlds largest known ferruginous basin, more than 50% of authigenic organic matter is degraded through methanogenesis, despite high abundances of Fe (hydr)oxides in the lake sediments. Biogenic CH₄ accumulates to high concentrations (up to 1.4 mmol L⁻¹) in the anoxic bottom waters, which contain a total of 7.4 × 10⁵ tons of CH₄. Profiles of dissolved inorganic carbon (ΣCO₂) and carbon isotopes (δ¹³C) show that CH₄ is oxidized in the vicinity of the persistent pycnocline and that some of this CH₄ is likely oxidized anaerobically. The dearth of NO₃⁻ and SO₄²⁻ in Lake Matano waters suggests that anaerobic methane oxidation may be coupled to the reduction of Fe (and/or Mn) (hydr)oxides. Thermodynamic considerations reveal that CH₄ oxidation coupled to Fe(III) or Mn(III/IV) reduction would yield sufficient free energy to support microbial growth at the substrate levels present in Lake Matano. Flux calculations imply that Fe and Mn must be recycled several times directly within the water column to balance the upward flux of CH₄. 16S gene cloning identified methanogens in the anoxic water column, and these methanogens belong to groups capable of both acetoclastic and hydrogenotrophic methanogenesis. We find that methane is important in C cycling, even in this very Fe-rich environment. Such Fe-rich environments are rare on Earth today, but they are analogous to conditions in the ferruginous oceans thought to prevail during much of the Archean Eon. By analogy, methanogens and methanotrophs could have formed an important part of the Archean Ocean ecosystem.

Green rust formation controls nutrient availability in a ferruginous water column

Iron-rich (ferruginous) conditions were a prevalent feature of the ocean throughout much of Earth’s history. The nature of elemental cycling in such settings is poorly understood, however, thus hampering reconstruction of paleoenvironmental conditions during key periods in Earth evolution. This is particularly true regarding controls on nutrient bioavailability, which is intimately linked to Earth’s oxygenation history. Elemental scavenging during precipitation of iron minerals exerts a major control on nutrient cycling in ferruginous basins, and the predictable nature of removal processes provides a mechanism for reconstructing ancient ocean chemistry. Such reconstructions depend, however, on precise knowledge of the iron minerals formed in the water column. Here, we combine mineralogical and geochemical analyses to demonstrate formation of the mixed-valence iron mineral, green rust, in ferruginous Lake Matano, Indonesia. Carbonated green rust (GR1), along with signifi cant amounts of magnetite, forms below the chemocline via the reduction of ferrihydrite. Further, we show that uptake of dissolved nickel, a key micronutrient required for methanogenesis, is signifi cantly enhanced during green rust formation, suggesting a major control on methane production in ancient ferruginous settings.

Deep‐water anoxygenic photosythesis in a ferruginous chemocline

Ferruginous Lake Matano, Indonesia hosts one of the deepest anoxygenic photosynthetic communities on Earth. This community is dominated by low-light adapted, BChl e-synthesizing green sulfur bacteria (GSB), which comprise ~25% of the microbial community immediately below the oxic-anoxic boundary (OAB; 115-120 m in 2010). The size of this community is dependent on the mixing regime within the lake and the depth of the OAB-at ~117 m, the GSB live near their low-light limit. Slow growth and C-fixation rates suggest that the Lake Matano GSB can be supported by sulfide even though it only accumulates to scarcely detectable (low μm to nm) concentrations. A model laboratory strain (Chlorobaculum tepidum) is indeed able to access HS- for oxidation at nm concentrations. Furthermore, the GSB in Lake Matano possess a full complement of S-oxidizing genes. Together, this physiological and genetic information suggests that deep-water GSB can be supported by a S-cycle, even under ferruginous conditions. The constraints we place on the metabolic capacity and physiology of GSB have important geobiological implications. Biomarkers diagnostic of GSB would be a good proxy for anoxic conditions but could not discriminate between euxinic and ferruginous states, and though GSB biomarkers could indicate a substantial GSB community, such a community may exist with very little metabolic activity. The light requirements of GSB indicate that at light levels comparable to those in the OAB of Lake Matano or the Black Sea, GSB would have contributed little to global ocean primary production, nutrient cycling, and banded iron formation (BIF) deposition in the Precambrian. Before the proliferation of oxygenic photosynthesis, shallower OABs and lower light absorption in the oceans surface waters would have permitted greater light availability to GSB, potentially leading to a greater role for GSB in global biogeochemical cycles.

Marinobacter bacteria associated with a massive sulphide ore deposit affect metal mobility in the deep subsurface

A microorganism of the Marinobacter genus capable of Fe-oxidation at near-neutral pH, both in the presence and absence of oxygen, was found at a depth of 1.4 km in proximity to a Cu-Zn Volcanogenic Massive Sulphide (VMS) deposit, within the Triple 7 mine, Flin Flon, Manitoba, Canada. The microorganism was isolated from saline groundwater emanating from boreholes at that depth, which contained a small microbial community consisting of only two organisms. To examine biogeochemical trace metal cycling in this deep subsurface setting, incubation experiments were carried out with the Marinobacter isolate and mineralized (metal-containing ore) material in batch and column flow-through settings. The activity of the Marinobacter isolate resulted in an increase in the mobilization of major elements (Fe, S) and trace metals (Cu, Zn) from the solid ore material. These results indicate that Fe-oxidation may be an important biogeochemical process in the deep subsurface, which affects the mobilization of Fe and trace elements from buried mineralization.