Kurt O. Konhauser

Could bacteria have formed the Precambrian banded iron formations

Banded iron formations (BIFs) are prominent sedimentary deposits of the Precambrian, but despite a century of endeavor, the mechanisms of their deposition are still unresolved. Interactions between microorganisms and dissolved ferrous iron in the ancient oceans offer one plausible means of mineral precipitation, in which bacteria directly generate ferric iron either by chemolithoautotrophic iron oxidation or by photoferrotrophy. On the basis of chemical analyses from BIF units of the 2.5 Ga Hamersley Group, Western Australia, we show here that even during periods of maximum iron precipitation, most, if not all, of the iron in BIFs could be precipitated by iron-oxidizing bacteria in cell densities considerably less than those found in modern Fe-rich aqueous environments. Those ancient microorganisms would also have been easily supported by the concentrations of nutrients (P) and trace metals (V, Mn, Co, Zn, and Mo) found within the same iron-rich bands. These calculations highlight the potential importance of early microbial activity on ancient metal cycling.

Diversity of bacterial iron mineralization

Abstract Bacterial cells, growing naturally in freshwater and marine environments or experimentally in culture, can precipitate a variety of authigenic iron minerals. With the vast majority of bacteria biomineralization is a two-step process: initially metals are electrostatically bound to the anionic surfaces of the cell wall and surrounding organic polymers, where they subsequently serve as nucleation sites for crystal growth. The biogenic minerals have crystal habits and chemical compositions similar to those produced by precipitation from inorganic solutions because they are governed by the same equilibrium principles that control mineralization of their inorganic counterparts. As the latter stages of mineralization are inorganically driven, the type of biomineral formed is inevitably dependent on the available counter-ions, and hence, the chemical composition of the waters in which the microorganisms are growing. In oxygenated waters, iron hydroxides are a common precipitate and can form passively through the binding of dissolved ferric species to negatively charged polymers or when soluble ferrous iron spontaneously reacts with dissolved oxygen to precipitate as ferric hydroxide on available nucleation sites (e.g. bacteria). Alternatively, the metabolic activity of Fe(II)-oxidizing bacteria can induce ferric hydroxide precipitation as a secondary by-product. Ferric hydroxide may then serve as a precursor for more stable iron oxides, such as goethite and hematite via dissolution–reprecipitation or dehydration, respectively, or it may react with dissolved silica, phosphate or sulphate to form other authigenic mineral phases. Under suboxic to anoxic conditions, ferric hydroxide may be converted to magnetite, siderite, and iron sulphides through various reductive processes associated with organic matter mineralization. Under biologically controlled conditions, where mineralization is completely regulated, magnetotactic bacteria form magnetite and greigite as navigational tools to guide themselves into their preferred habitat. In general, the formation of iron biominerals is not difficult to achieve, bacteria simply provide charged surfaces that bind metals and they excrete metabolic waste products into the surrounding environment that induce mineralization. The ubiquitous presence of bacteria in aquatic systems and their inherent ability to biomineralize, therefore, makes them extremely important agents in driving both modern and ancient geochemical cycles.

Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria

The mechanism of banded iron formation (BIF) deposition is controversial, but classically has been interpreted to reflect ferrous iron [Fe(II)] oxidation by molecular oxygen after cyanobacteria evolved on Earth. Anoxygenic photoautotrophic bacteria can also catalyze Fe(II) oxidation under anoxic conditions. Calculations based on experimentally determined Fe(II) oxidation rates by these organisms under light regimes representative of ocean water at depths of a few hundred meters suggest that, even in the presence of cyanobacteria, anoxygenic phototrophs living beneath a wind-mixed surface layer provide the most likely explanation for BIF deposition in a stratified ancient ocean and the absence of Fe in Precambrian surface waters.

Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event

It has been suggested that a decrease in atmospheric methane levels triggered the progressive rise of atmospheric oxygen, the so-called Great Oxidation Event, about 2.4 Gyr ago. Oxidative weathering of terrestrial sulphides, increased oceanic sulphate, and the ecological success of sulphate-reducing microorganisms over methanogens has been proposed as a possible cause for the methane collapse, but this explanation is difficult to reconcile with the rock record. Banded iron formations preserve a history of Precambrian oceanic elemental abundance and can provide insights into our understanding of early microbial life and its influence on the evolution of the Earth system. Here we report a decline in the molar nickel to iron ratio recorded in banded iron formations about 2.7 Gyr ago, which we attribute to a reduced flux of nickel to the oceans, a consequence of cooling upper-mantle temperatures and decreased eruption of nickel-rich ultramafic rocks at the time. We measured nickel partition coefficients between simulated Precambrian sea water and diverse iron hydroxides, and subsequently determined that dissolved nickel concentrations may have reached ∼400 nM throughout much of the Archaean eon, but dropped below ∼200 nM by 2.5 Gyr ago and to modern day values (∼9 nM) by ∼550 Myr ago. Nickel is a key metal cofactor in several enzymes of methanogens and we propose that its decline would have stifled their activity in the ancient oceans and disrupted the supply of biogenic methane. A decline in biogenic methane production therefore could have occurred before increasing environmental oxygenation and not necessarily be related to it. The enzymatic reliance of methanogens on a diminishing supply of volcanic nickel links mantle evolution to the redox state of the atmosphere.

Diversity of iron and silica precipitation by microbial mats in hydrothermal waters, Iceland: Implications for Precambrian iron formations

Direct examination of microbial mats from Icelandic hot springs with transmission electron microscopy and energy-dispersive X-ray spectroscopy revealed a consortium of bacterial cells in varying stages of mineralization. Differences in observed mineralogy largelyreflectdifferencesinthechemistryofthehydrothermalwaters.Silica-richspheroids formedepicellularlyoncellwallsandsurroundingsheathsandcapsulesofmicroorganisms and,insomecases,intracellularlywhenpresumablythecell(s)hadlysed.Commonly,these precipitateswereobservedcoalescingtoformamatrixofamorphoussilicathatcompletely encapsulated the cells and/or replaced their cytoplasmic material. However, in other cells, the precipitates were composed of amorphous granules made exclusively of iron and silica inapproximatelyequalproportions.Atonelocality,thebacteriaformedseveralepicellular iron minerals, ranging from iron-mineralized capsules tofine-grained spheroids of amorphous ferric hydroxide and acicular aggregates of goethite. The complete encrustation of bacterial cells by silica, iron, or a combination of both may greatly enhance their preservation potential, such that these mineralized microorganisms may conceivably represent future microfossils. Thus, we may be witnessing contemporaneous biomineralization processes that are similar to those of the geologic past, particularly with regard to the origin of some Precambrian banded iron formations.

Proterozoic ocean redox and biogeochemical stasis

The partial pressure of oxygen in Earth’s atmosphere has increased dramatically through time, and this increase is thought to have occurred in two rapid steps at both ends of the Proterozoic Eon (∼2.5–0.543 Ga). However, the trajectory and mechanisms of Earth’s oxygenation are still poorly constrained, and little is known regarding attendant changes in ocean ventilation and seafloor redox. We have a particularly poor understanding of ocean chemistry during the mid-Proterozoic (∼1.8–0.8 Ga). Given the coupling between redox-sensitive trace element cycles and planktonic productivity, various models for mid-Proterozoic ocean chemistry imply different effects on the biogeochemical cycling of major and trace nutrients, with potential ecological constraints on emerging eukaryotic life. Here, we exploit the differing redox behavior of molybdenum and chromium to provide constraints on seafloor redox evolution by coupling a large database of sedimentary metal enrichments to a mass balance model that includes spatially variant metal burial rates. We find that the metal enrichment record implies a Proterozoic deep ocean characterized by pervasive anoxia relative to the Phanerozoic (at least ∼30–40% of modern seafloor area) but a relatively small extent of euxinic (anoxic and sulfidic) seafloor (less than ∼1–10% of modern seafloor area). Our model suggests that the oceanic Mo reservoir is extremely sensitive to perturbations in the extent of sulfidic seafloor and that the record of Mo and chromium enrichments through time is consistent with the possibility of a Mo–N colimited marine biosphere during many periods of Earth’s history.

The evolution of the marine phosphate reservoir

Phosphorus is a biolimiting nutrient that has an important role in regulating the burial of organic matter and the redox state of the ocean–atmosphere system. The ratio of phosphorus to iron in iron-oxide-rich sedimentary rocks can be used to track dissolved phosphate concentrations if the dissolved silica concentration of sea water is estimated. Here we present iron and phosphorus concentration ratios from distal hydrothermal sediments and iron formations through time to study the evolution of the marine phosphate reservoir. The data suggest that phosphate concentrations have been relatively constant over the Phanerozoic eon, the past 542 million years (Myr) of Earth’s history. In contrast, phosphate concentrations seem to have been elevated in Precambrian oceans. Specifically, there is a peak in phosphorus-to-iron ratios in Neoproterozoic iron formations dating from ∼750 to ∼635 Myr ago, indicating unusually high dissolved phosphate concentrations in the aftermath of widespread, low-latitude ‘snowball Earth’ glaciations. An enhanced postglacial phosphate flux would have caused high rates of primary productivity and organic carbon burial and a transition to more oxidizing conditions in the ocean and atmosphere. The snowball Earth glaciations and Neoproterozoic oxidation are both suggested as triggers for the evolution and radiation of metazoans. We propose that these two factors are intimately linked; a glacially induced nutrient surplus could have led to an increase in atmospheric oxygen, paving the way for the rise of metazoan life.

Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event

The enrichment of redox-sensitive trace metals in ancient marine sedimentary rocks has been used to determine the timing of the oxidation of the Earth’s land surface. Chromium (Cr) is among the emerging proxies for tracking the effects of atmospheric oxygenation on continental weathering; this is because its supply to the oceans is dominated by terrestrial processes that can be recorded in the Cr isotope composition of Precambrian iron formations. However, the factors controlling past and present seawater Cr isotope composition are poorly understood. Here we provide an independent and complementary record of marine Cr supply, in the form of Cr concentrations and authigenic enrichment in iron-rich sedimentary rocks. Our data suggest that Cr was largely immobile on land until around 2.48 Gyr ago, but within the 160 Myr that followed—and synchronous with independent evidence for oxygenation associated with the Great Oxidation Event (see, for example, refs 4–6)—marked excursions in Cr content and Cr/Ti ratios indicate that Cr was solubilized at a scale unrivalled in history. As Cr isotope fractionations at that time were muted, Cr must have been mobilized predominantly in reduced, Cr(iii), form. We demonstrate that only the oxidation of an abundant and previously stable crustal pyrite reservoir by aerobic-respiring, chemolithoautotrophic bacteria could have generated the degree of acidity required to solubilize Cr(iii) from ultramafic source rocks and residual soils. This profound shift in weathering regimes beginning at 2.48 Gyr ago constitutes the earliest known geochemical evidence for acidophilic aerobes and the resulting acid rock drainage, and accounts for independent evidence of an increased supply of dissolved sulphate and sulphide-hosted trace elements to the oceans around that time. Our model adds to amassing evidence that the Archaean-Palaeoproterozoic boundary was marked by a substantial shift in terrestrial geochemistry and biology.

Bacterial clay authigenesis: a common biogeochemical process

Abstract Transmission electron microscopic (TEM) analyses of freshwater biofilms and bacterial cells, grown in experimental culture, have shown that these microorganisms are commonly associated with fine-grained (Fe, Al)-silicates of variable composition. The inorganic phases develop in a predictable manner, beginning with the adsorption of cationic iron to anionic cellular surfaces, supersaturation of the proximal fluid with Fe3+, nucleation and precipitation of a precursor ferric hydroxide phase on the cell surface, followed by reaction with dissolved silica and aluminum and eventually the growth of an amorphous clay-like phase. Alternatively, colloidal species of (Fe, Al)-silicate composition may react directly with either the anionic cellular polymers or adsorbed iron, depending on their net charge. Over time, these hydrous precursors may dehydrate and convert to more stable crystalline phases. Because microbial biofilms are expansive and highly reactive surfaces at the sediment–water interface, coupled with their ability to bind soluble components and form solid inorganic phases, they should influence the chemical composition of the overlying aqueous microenvironment, and ultimately contribute to the makeup of river bottom sediment.

The effect of cyanobacteria on silica precipitation at neutral pH: implications for bacterial silicification in geothermal hot springs

In this study, we performed silica precipitation experiments with the cyanobacteria Calothrix sp. to investigate the mechanisms of silica biomineralization. Batch silica precipitation experiments were conducted at neutral pH as a function of time, Si saturation states, temperature and ferrihydrite concentrations. The experimental results show that in solutions undersaturated with respect to amorphous silica, the interaction between Si and cell surface functional groups is weak and minimal Si sorption onto cyanobacterial surfaces occurs. In solutions at high Si supersaturation states, abiotic Si polymerization is spontaneous, and at the time scales of our experiments (1–50 h) the presence of cyanobacteria had a negligible effect on silica precipitation kinetics. At lower supersaturation states, Si polymerization is slow and the presence of cyanobacteria do not promote Si–solid phase nucleation. In contrast, experiments conducted with ferrihydrite-coated cyanobacteria significantly increase the rate of Si removal, and the extent to which Si is removed increases as a function of ferrihydrite concentration. Experiments conducted with inorganic ferrihydrite colloids (without cyanobacteria) removes similar amounts of Si, suggesting that microbial surfaces play a limited role in the silica precipitation process. Therefore, in supersaturated hydrothermal waters, silica precipitation is largely nonbiogenic and cyanobacterial surfaces have a negligible effect on silica nucleation. D 2003 Elsevier Science B.V. All rights reserved.