Mesophilic microorganisms build terrestrial mats analogous to Precambrian microbial jungles.

Development of Archean paleosols and patterns of Precambrian rock weathering suggest colonization of continents by subaerial microbial mats long before evolution of land plants in the Phanerozoic Eon. Modern analogues for such mats, however, have not been reported, and possible biogeochemical roles of these mats in the past remain largely conceptual. We show that photosynthetic, subaerial microbial mats from Indonesia grow on mafic bedrocks at ambient temperatures and form distinct layers with features similar to Precambrian mats and paleosols. Such subaerial mats could have supported a substantial aerobic biosphere, including nitrification and methanotrophy, and promoted methane emissions and oxidative weathering under ostensibly anoxic Precambrian atmospheres. High C-turnover rates and cell abundances would have made these mats prime locations for early microbial diversification. Growth of landmass in the late Archean to early Proterozoic Eons could have reorganized biogeochemical cycles between land and sea impacting atmospheric chemistry and climate.

Shifting microbial communities sustain multiyear iron reduction and methanogenesis in ferruginous sediment incubations.

Reactive Fe(III) minerals can influence methane (CH4 ) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH4 oxidation. The balance between Fe(III) reduction, methanogenesis, and CH4 oxidation in ferruginous Archean and Paleoproterozoic oceans would have controlled CH4 fluxes to the atmosphere, thereby regulating the capacity for CH4 to warm the early Earth under the Faint Young Sun. We studied CH4 and Fe cycling in anoxic incubations of ferruginous sediment from the ancient ocean analogue Lake Matano, Indonesia, over three successive transfers (500 days in total). Iron reduction, methanogenesis, CH4 oxidation, and microbial taxonomy were monitored in treatments amended with ferrihydrite or goethite. After three dilutions, Fe(III) reduction persisted only in bottles with ferrihydrite. Enhanced CH4 production was observed in the presence of goethite, highlighting the potential for reactive Fe(III) oxides to inhibit methanogenesis. Supplementing the media with hydrogen, nickel and selenium did not stimulate methanogenesis. There was limited evidence for Fe(III)-dependent CH4 oxidation, although some incubations displayed CH4 -stimulated Fe(III) reduction. 16S rRNA profiles continuously changed over the course of enrichment, with ultimate dominance of unclassified members of the order Desulfuromonadales in all treatments. Microbial diversity decreased markedly over the course of incubation, with subtle differences between ferrihydrite and goethite amendments. These results suggest that Fe(III) oxide mineralogy and availability of electron donors could have led to spatial separation of Fe(III)-reducing and methanogenic microbial communities in ferruginous marine sediments, potentially explaining the persistence of CH4 as a greenhouse gas throughout the first half of Earth history.

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 ocean's surface waters would have permitted greater light availability to GSB, potentially leading to a greater role for GSB in global biogeochemical cycles.

The methane cycle in ferruginous Lake Matano.

In Lake Matano, Indonesia, the world's 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 SO4²â» 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.

Alteration of iron-rich lacustrine sediments by dissimilatory iron-reducing bacteria.

The reduction of Fe during bacterial anaerobic respiration in sediments and soils not only causes the degradation of organic matter but also results in changes in mineralogy and the redistribution of many nutrients and trace metals. Understanding trace metal patterns in sedimentary rocks and predicting the fate of contaminants in the environment requires a detailed understanding of the mechanisms through which they are redistributed during Fe reduction. In this work, lacustrine sediments from Lake Matano in Indonesia were incubated in a minimal media with the dissimilatory iron reducing (DIR) bacterium Shewanella putrefaciens 200R. These sediments were reductively dissolved at rates slower than pure synthetic goethite despite the presence of an 'easily reducible' component, as defined by selective extractions. DIR of the lacustrine sediments resulted in the substrate-dependent production of abundant quantities of extracellular polymeric substances. Trace elements, including Ni, Co, P, Si, and As, were released from the sediments with progressive Fe reduction while Cr was sequestered. Much of the initial trace metal mobility can be attributed to the rapid reduction of a Mn-rich oxyhydroxide phase. The production of organo-Fe(III) reveals that DIR bacteria can generate significant metal complexation capacity. This work demonstrates that DIR induces the release of many elements associated with Fe-Mn oxyhydroxides, despite secondary mineralization.

XAFS determination of the bacterial cell wall functional groups responsible for complexation of Cd and U as a function of pH.

Bacteria, which are ubiquitous in near-surface geologic systems, can affect the distribution and fate of metals in these systems through adsorption reactions between the metals and bacterial cell walls. Recently, Fein et al. (1997) developed a chemical equilibrium approach to quantify metal adsorption onto cell walls, treating the sorption as a surface complexation phenomenon. However, such models are based on circumstantial bulk adsorption evidence only, and the nature and mechanism of metal binding to cell walls for each metal system have not been determined spectroscopically. The results of XAFS measurements at the Cd K-edge and U L3-edge on Bacillus subtilis exposed to these elements show that, at low pH, U binds to phosphoryl groups while Cd binds to carboxyl functional groups.

Comparison of the structures of the metal-thiolate binding site in Zn(II)-, Cd(II)-, and Hg(II)-metallothioneins using molecular modeling techniques.

The first fully energy-minimized structures for a series of structurally related metal complexes of the important mammalian metal binding protein metallothionein are described. The structures were calculated based on structural information obtained from existing spectroscopic and crystallographic data, and minimized using molecular mechanics (MM2) techniques. A two domain structure, with stoichiometries of M(II)3-(Scys)9 and M(II)4-(Scys)11 where M = zinc(II), cadmium(II), and mercury(II), was assembled and minimized. The resultant three-dimensional structure closely resembled that of rat liver Cd5Zn2-MT 1 obtained by analysis of x-ray diffraction data [A. H. Robbins, D.E. McRee, M. Williamson, S. A. Collett, N. H. Xuong, W. F. Furey, B. C. Wang and C. D. Stout, J. Mol. Biol. 221, 1269-1293 (1991)]. Minimized structures for Zn7-MT, Cd7-MT, and Hg7-MT are reported. Deep crevices that expose the metal-thiolate clusters are seen in each structure. However, for the mercury-containing protein, much of the mercury-thiolate structure is visible and it is proposed that this provides access for extensive interaction between solvent water molecules and the mercury(II), resulting in the observed distortion away from tetrahedral geometry for Hg7-MT. Volume calculations are reported for the protein metallated with 7 Zn(II), Cd(II), or Hg(II). A series of structural changes calculated for the step-wise isomorphous replacement of Zn(II) by Cd(II) and Hg(II) in the Zn4S11 alpha domain are shown.