The methane cycle in ferruginous Lake Matano (original) (raw)
Related papers
The methane cycle in tropical Lake Matano: An analogue for Precambrian methane cycling?
2008
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 CH 4 accumulates to high concentrations (up to 1.4 mmol L )1 ) in the anoxic bottom waters, which contain a total of 7.4 · 10 5 tons of CH 4 . Profiles of dissolved inorganic carbon (RCO 2 ) and carbon isotopes (d 13 C) show that CH 4 is oxidized in the vicinity of the persistent pycnocline and that some of this CH 4 is likely oxidized anaerobically. The dearth of NO 3 ) and SO 4 2) 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 CH 4 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 CH 4 . 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.
Geology , 2024
The greenhouse gas methane (CH 4) contributed to a warm climate that maintained liquid water and sustained Earth's habitability in the Precambrian despite the faint young sun. The viability of methanogenesis (ME) in ferruginous environments, however, is debated, as iron reduction can potentially outcompete ME as a pathway of organic carbon remineralization (OCR). Here, we document that ME is a dominant OCR process in Brownie Lake, Minnesota (midwestern United States), which is a ferruginous (iron-rich, sulfate-poor) and meromictic (stratified with permanent anoxic bottom waters) system. We report ME accounting for ≥90% and >9% ± 7% of the anaerobic OCR in the water column and sediments, respectively, and an overall particulate organic carbon loading to CH 4 conversion efficiency of ≥18% ± 7% in the anoxic zone of Brownie Lake. Our results, along with previous reports from ferruginous systems, suggest that even under low primary productivity in Precambrian oceans, the efficient conversion of organic carbon would have enabled marine CH 4 to play a major role in early Earth's biogeochemical evolution.
Iron‐mediated anaerobic ammonium oxidation recorded in the early Archean ferruginous ocean
Geobiology
The nitrogen isotopic composition of organic matter is controlled by metabolic activity and redox speciation and has therefore largely been used to uncover the early evolution of life and ocean oxygenation. Specifically, positive δ15N values found in well‐preserved sedimentary rocks are often interpreted as reflecting the stability of a nitrate pool sustained by water column partial oxygenation. This study adds much‐needed data to the sparse Paleoarchean record, providing carbon and nitrogen concentrations and isotopic compositions for more than fifty samples from the 3.4 Ga Buck Reef Chert sedimentary deposit (BRC, Barberton Greenstone Belt). In the overall anoxic and ferruginous conditions of the BRC depositional environment, these samples yield positive δ15N values up to +6.1‰. We argue that without a stable pool of nitrates, these values are best explained by non‐quantitative oxidation of ammonium via the Feammox pathway, a metabolic co‐cycling between iron and nitrogen through ...
Modulation of oxygen production in Archaean oceans by episodes of Fe(II) toxicity
Nature Geoscience, 2015
Oxygen accumulated in the surface waters of the Earth's oceans 1 and atmosphere 2 several hundred million years before the Great Oxidation Event between 2.4 and 2.3 billion years ago 3 . Before the Great Oxidation Event, periods of enhanced submarine volcanism associated with mantle plume events 4 supplied Fe(II) to sea water. These periods generally coincide with the disappearance of indicators of the presence of molecular oxygen in Archaean sedimentary records 5 . The presence of Fe(II) in the water column can lead to oxidative stress in some organisms as a result of reactions between Fe(II) and oxygen that produce reactive oxygen species 6 . Here we test the hypothesis that the upwelling of Fe(II)-rich, anoxic water into the photic zone during the late Archaean subjected oxygenic phototrophic bacteria to Fe(II) toxicity. In laboratory experiments, we found that supplying Fe(II) to the anoxic growth medium housing a common species of planktonic cyanobacteria decreased both the e ciency of oxygenic photosynthesis and their growth rates. We suggest that this occurs because of increasing intracellular concentrations of reactive oxygen species. We use geochemical modelling to show that Fe(II) toxicity in conditions found in the late Archaean photic zone could have substantially inhibited water column oxygen production, thus decreasing fluxes of oxygen to the atmosphere. We therefore propose that the timing of atmospheric oxygenation was controlled by the timing of submarine, plumetype volcanism, with Fe(II) toxicity as the modulating factor.
Iron-dependent nitrogen cycling in a ferruginous lake and the nutrient status of Proterozoic oceans
Nature Geoscience, 2017
Nitrogen limitation during the Proterozoic has been inferred from the great expanse of ocean anoxia under low-O 2 atmospheres, which could have promoted NO 3 − reduction to N 2 and fixed N loss from the ocean. The deep oceans were Fe rich (ferruginous) during much of this time, yet the dynamics of N cycling under such conditions remain entirely conceptual, as analogue environments are rare today. Here we use incubation experiments to show that a modern ferruginous basin, Kabuno Bay in East Africa, supports high rates of NO 3 − reduction. Although 60% of this NO 3 − is reduced to N 2 through canonical denitrification, a large fraction (40%) is reduced to NH 4 + , leading to N retention rather than loss. We also find that NO 3 − reduction is Fe dependent, demonstrating that such reactions occur in natural ferruginous water columns. Numerical modelling of ferruginous upwelling systems, informed by our results from Kabuno Bay, demonstrates that NO 3 − reduction to NH 4 + could have enhanced biological production, fuelling sulfate reduction and the development of mid-water euxinia overlying ferruginous deep oceans. This NO 3 − reduction to NH 4 + could also have partly o set a negative feedback on biological production that accompanies oxygenation of the surface ocean. Our results indicate that N loss in ferruginous upwelling systems may not have kept pace with global N fixation at marine phosphorous concentrations (0.04-0.13 µM) indicated by the rock record. We therefore suggest that global marine biological production under ferruginous ocean conditions in the Proterozoic eon may thus have been P not N limited.
Frontiers in Microbiology, 2016
Lakes represent a considerable natural source of methane to the atmosphere compared to their small global surface area. Methanotrophs in sediments and in the water column largely control methane fluxes from these systems, yet the diversity, electron accepting capacity, and nutrient requirements of these microorganisms have only been partially identified. Here, we investigated the role of electron acceptors alternative to oxygen and sulfate in microbial methane oxidation at the oxycline and in anoxic waters of the ferruginous meromictic Lake La Cruz, Spain. Active methane turnover in a zone extending well below the oxycline was evidenced by stable carbon isotope-based rate measurements. We observed a strong methane oxidation potential throughout the anoxic water column, which did not vary substantially from that at the oxic/anoxic interface. Both in the redox-transition and anoxic zones, only aerobic methane-oxidizing bacteria (MOB) were detected by fluorescence in situ hybridization and sequencing techniques, suggesting a close coupling of cryptic photosynthetic oxygen production and aerobic methane turnover. Additions of nitrate, nitrite and to a lesser degree iron and manganese oxides also stimulated bacterial methane consumption. We could not confirm a direct link between the reduction of these compounds and methane oxidation and we cannot exclude the contribution of unknown anaerobic methanotrophs. Nevertheless, our findings from Lake La Cruz support recent laboratory evidence that aerobic methanotrophs may be able to utilize alternative terminal electron acceptors under oxygen limitation.
Iron-oxidizing microbial ecosystems thrived in late Paleoproterozoic redox-stratified oceans
Earth and Planetary Science Letters, 2009
We conducted a geochemical and petrographic study of the 1.89 billion year old Gunflint and Biwabik iron formations, with the goal of determining the importance of microbial iron-oxidation in the formation of ironand microfossil-rich stromatolites. We used redox-sensitive tracers, such as iron isotopes and rare earth elements, to decipher whether these ancient microbial ecosystems harbored cyanobacteria or Fe-oxidizing bacteria as primary producers. Iron-rich stromatolites contain non-significant or positive Ce anomalies, which contrast with shallow water deposits having negative Ce anomalies. This trend in Ce anomalies indicates that the stromatolites formed in low oxygen conditions, which is the ideal setting for the proliferation of Fe-oxidizing bacterial ecosystems. The stromatolites yield a large range of δ 56 Fe values, from −0.66 to +0.82‰, but contain predominantly positive values indicating the prevalence of partial Feoxidation. Based on modern analogues, Fe-oxides precipitated in cyanobacterial mats are expected to record an isotopic signature of quantitative oxidation, which in marine settings will yield negative δ 56 Fe values. The stromatolite iron isotope data, therefore, provide evidence for the presence of Fe-oxidizing bacteria. The stromatolites can be traced for a distance of over 100 km in these iron formations, indicating that they record a pervasive rather than localized ecosystem. Their preservation in late Paleoproterozoic successions deposited along the margins of the Superior craton suggests that there was a global expansion of ironoxidizing bacterial communities at shallow-water redox boundaries in late Paleoproterozoic oceans.
Iron oxide reactivity controls organic matter mineralization in ferruginous sediments
2020
Ferruginous sediments were widespread during the Archaean and Proterozoic Eons, but our knowledge about organic matter mineralization remains mostly conceptual, as analogous modern ferruginous sediments are largely unstudied. In sediments of ferruginous Lake Towuti, Indonesia, methanogenesis dominates organic matter mineralization despite abundant reactive ferric iron phases persisting throughout the core. This implies that ferric iron can be buried over geologic timescales even in the presence of labile organic carbon. Iron reactivity and hence its contribution to organic matter mineralization is highly variable. With negligible methane oxidation, methane may diffuse from the sediment into the water column and reach the atmosphere. We hypothesize that similar conditions prevailed during the Archaean and Proterozoic Eons, and thus, may have contributed to regulating Earth’s early climate.
Organic matter mineralization in modern and ancient ferruginous sediments
Nature Communications
Deposition of ferruginous sediment was widespread during the Archaean and Proterozoic Eons, playing an important role in global biogeochemical cycling. Knowledge of organic matter mineralization in such sediment, however, remains mostly conceptual, as modern ferruginous analogs are largely unstudied. Here we show that in sediment of ferruginous Lake Towuti, Indonesia, methanogenesis dominates organic matter mineralization despite highly abundant reactive ferric iron phases like goethite that persist throughout the sediment. Ferric iron can thus be buried over geologic timescales even in the presence of labile organic carbon. Coexistence of ferric iron with millimolar concentrations of methane further demonstrates lack of iron-dependent methane oxidation. With negligible methane oxidation, methane diffuses from the sediment into overlying waters where it can be oxidized with oxygen or escape to the atmosphere. In low-oxygen ferruginous Archaean and Proterozoic oceans, therefore, sedi...