Photoferrotrophy, the process by which inorganic carbon is fixed into organic matter using light as an energy source and reduced iron [Fe(II)] as an electron donor, has been proposed as one of the oldest photoautotrophic metabolisms on Earth. Under the iron-rich (ferruginous) but sulfide poor conditions dominating the Archean ocean, this type of metabolism could have accounted for most of the primary production in the photic zone. Here we review the current knowledge of biogeochemical, microbial and phylogenetic aspects of photoferrotrophy, and evaluate the ecological significance of this process in ancient and modern environments. From the ferruginous conditions that prevailed during most of the Archean, the ancient ocean evolved toward euxinic (anoxic and sulfide rich) conditions and, finally, much after the advent of oxygenic photosynthesis, to a predominantly oxic environment. Under these new conditions photoferrotrophs lost importance as primary producers, and now photoferrotrophy remains as a vestige of a formerly relevant photosynthetic process. Apart from the geological record and other biogeochemical markers, modern environments resembling the redox conditions of these ancient oceans can offer insights into the past significance of photoferrotrophy and help to explain how this metabolism operated as an important source of organic carbon for the early biosphere. Iron-rich meromictic (permanently stratified) lakes can be considered as modern analogs of the ancient Archean ocean, as they present anoxic ferruginous water columns where light can still be available at the chemocline, thus offering suitable niches for photoferrotrophs. A few bacterial strains of purple bacteria as well as of green sulfur bacteria have been shown to possess photoferrotrophic capacities, and hence, could thrive in these modern Archean ocean analogs. Studies addressing the occurrence and the biogeochemical significance of photoferrotrophy in ferruginous environments have been conducted so far in lakes Matano, Pavin, La Cruz, and the Kabuno Bay of Lake Kivu. To date, only in the latter two lakes a biogeochemical role of photoferrotrophs has been confirmed. In this review we critically summarize the current knowledge on iron-driven photosynthesis, as a remains of ancient Earth biogeochemistry.

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Photoferrotrophy: Remains of an Ancient Photosynthesis in Modern Environments.

In the.590-m deep, tropical Lake Matano (Indonesia), stratification is characterized by weak thermal gradients (,2uC per 500 m) and weak salinity gradients (,0.14%per 500 m). These gradients persist over seasons, decades, and possibly centuries. Under these nearly steady-state conditions, vertical eddy diffusion coefficients (K z ) cannot be estimated by conventional methods that rely on time derivatives of temperature distributions. We use and compare several alternative methods: one-dimensionalk‐emodeling, three-dimensional hydrodynamic modeling, correlation with the size of Thorpe instabilities, and correlation with the stability frequency. In the thermocline region, at 100-m depth, theK z is,5310 26 m 2 s 21 , but, below 300 m, the small density gradient results in large (20 m) vertical eddies and high mixing rates (K z ,10 22 m 2 s 21 ). The estimated timescale of water renewal in the monimolimnion is several hundred years. Intense evaporation depletes the surface mixed layer of 16 O and 1 H isotopes, making it isotopically heavier. The lake waters become progressively isotopically lighter with depth, and the isotopic composition in the deep waters is close to those of the ground and tributary waters. The vertical distribution ofK z is used in a biogeochemical reaction‐transport model. We show that, outside of a narrow thermocline region, the vertical distributions of dissolved oxygen, iron, methane, and phosphorus are shaped by vertical variations in transport rates, rather than by sources or sinks.

https://kuscholarworks.ku.edu/bitstream/handle/1808/16953/FowleD_LO_55(2)763.pdf;sequence=1

Mixing and its effects on biogeochemistry in the persistently stratified, deep, tropical Lake Matano, Indonesia

Lakes turn meromictic, when mixing and deep recirculation are insufficient to homogenize the water body and remove chemical gradients. A deepwater layer “the monimolimnion ” is excluded from the deep recirculation and hence develops a pronounced different chemical milieu. It persists through all seasons due to its high density. A limited number of processes are known to accomplish such a density increase of the deep water to create meromixis , such as salty inflows and partial deepwater renewal . However, also geochemical processes, such as decomposition of organic material, iron oxidation, and redissolution and calcite precipitation, can be responsible for meromixis. Other than the overlying water layer “the mixolimnion, ” the monimolimnion does not get into direct contact with the atmosphere and hence is not directly supplied with oxygen. Other substances can be enriched by precipitation and flocculation from the mixolimnion until the solubility product is reached or gas pressure grows beyond absolute pressure. As a consequence, the composition of solutes deviates clearly from usual water composition, and quantitative approaches for density must implement appropriate numerical approaches. The permanent density stratification limits the vertical transport of water and solutes. In several lakes, double-diffusive convection has been reported to significantly enhance the vertical solute transport.

Physical Features of Meromictic Lakes: Stratification and Circulation

Lake Matano, Indonesia, is a stratified anoxic lake with iron-rich waters that has been used as an analogue for the Archean and early Proterozoic oceans. Past studies of Lake Matano report large amounts of methane production, with as much as 80% of primary production degraded via methanogenesis. Low δ(13)C values of DIC in the lake are difficult to reconcile with this notion, as fractionation during methanogenesis produces isotopically heavy CO2. To help reconcile these observations, we develop a box model of the carbon cycle in ferruginous Lake Matano, Indonesia, that satisfies the constraints of CH4 and DIC isotopic profiles, sediment composition, and alkalinity. We estimate methane fluxes smaller than originally proposed, with about 9% of organic carbon export to the deep waters degraded via methanogenesis. In addition, despite the abundance of Fe within the waters, anoxic ferric iron respiration of organic matter degrades <3% of organic carbon export, leaving methanogenesis as the largest contributor to anaerobic organic matter remineralization, while indicating a relatively minor role for iron as an electron acceptor. As the majority of carbon exported is buried in the sediments, we suggest that the role of methane in the Archean and early Proterozoic oceans is less significant than presumed in other studies.

Modeling the carbon cycle in Lake Matano

The diffusive regime of double-diffusive convection generates staircases consisting of thin high-gradient interfaces sandwiched between convectively mixed layers. Simultaneous microstructure measurements of both temperature and conductivity from the staircases in Lake Kivu are used to test flux laws and theoretical models for double diffusion. Density ratios in Lake Kivu are between one and ten and mixed layer thicknesses on average 0.7 m. The larger interface thickness of temperature (average 9 cm) compared to dissolved substances (6 cm) confirms the boundary-layer structure of the interface. Our observations suggest that the boundary-layer break-off cannot be characterized by a single critical boundary-layer Rayleigh number, but occurs within a range of O(10(2)) to O(10(4)). Heat flux parameterizations which assume that the Nusselt number follows a power law increase with the Rayleigh number Ra are tested for their exponent . In contrast to the standard estimate =1/3, we found =0.200.03 for density ratios between two and six. Therefore, we suggest a correction of heat flux estimates which are based on =1/3. The magnitude of the correction depends on Ra in the system of interest. For Lake Kivu (average heat flux 0.10 W m(-2)) with Ra=O(10(8)), corrections are marginal. In the Arctic Ocean with Ra=O(10(8)) to O(10(12)), however, heat fluxes can be overestimated by a factor of four.

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Interface structure and flux laws in a natural double-diffusive layering

[1] From a small meromictic lake, we present observations of a circulation pattern that has not been documented in the limnological literature before. While surface cooling drives a vertical circulation of the upper water layer (mixolimnion), the deeper water layer (monimolimnion) is not included because of its higher salt concentration. However, double diffusion (higher diffusivity of heat than of dissolved substances) facilitates the faster escape of heat from the monimolimnion compared to dissolved substances during cold periods. As a consequence, interfacial cooling drives a vertical circulation within the monimolimnion without breaking the stratification toward the mixolimnion. In the presented case, the geochemical setting does not permit dissolved substances to accumulate in the mixolimnion. As a consequence, the system approaches the case of two immiscible layers in thermal contact. Below the interface, a convection layer is formed that exceeds the staircase layer thickness of double diffusion when conservative salts are involved. Finally, the entire lake circulates as two separate convection layers. This has a decisive impact on the formation of gradients and the redistribution of dissolved substances in lakes.

https://agupubs.onlinelibrary.wiley.com/doi/pdf/10.1029/2009GC002389

Sandra Naujoks

Papers

Double-diffusive deep water circulation in an iron-meromictic lake