Photoferrotrophy: Remains of an Ancient Photosynthesis in Modern Environments

Abstract

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.

Keywords: Archean ocean; anoxygenic phototrophs; evolution; ferruginous conditions; iron-rich meromictic lakes; photoferrotrophy.

FIGURE 1

Geochemical changes from the Archean to the Proterozoic ocean. (A) Time before present in Giga years (Ga), where color gradients denote postulated changes in deep-sea redox conditions. (B) Schematic distribution of reduced iron [Fe(II)], sulfide (H₂S) and oxygen in the water column of the ocean at each period. (C) Periods of banded iron formation (BIF) deposition where the bar width represents the postulated amount of BIF precipitation. Diagram compiled and modified from Anbar and Knoll (2002), Knoll (2003), and Canfield et al. (2008).

FIGURE 2

Model for BIF formation on the continental shelf. Deep anoxic water, rich in dissolved Fe(II) of hydrothermal origin, is transported onto the continental shelf, where Fe(II) gets oxidized. The produced oxides precipitate from solution toward the seafloor, in association with diverse components such as silica, carbonates or organic matter. The oxidation mechanisms are still unknown and could include a chemical reaction with dissolved O₂, a UV-light mediated photo-oxidation (less probable), a biological iron-oxidation by anoxygenic photosynthesis using Fe(II) as electron donor, or a combination of the above mentioned processes. Illustration compiled from Konhauser et al. (2002, 2007a), Kappler et al. (2005), Canfield et al. (2006), Severmann et al. (2008), Blake et al. (2010), and Tangalos et al. (2010).

FIGURE 3

(A) Physical and chemical features, anoxygenic phototrophic bacteria biomass, and anoxygenic inorganic carbon assimilation in the vertical profile of Lake La Cruz. The two charts on the right correspond to a zoom of the grey area of those on the left (symbols and lines used are the same for the same variable) (B) Photograph of Lake La Cruz and (C) light spectral penetration at various depths of the water column. Redrawn from Picazo (2016).

FIGURE 4

(A) In situ anoxygenic phototrophic (DCMU amended batches) inorganic carbon uptake in samples from the chemocline of Lake La Cruz amended with Fe(II), NO₃^-, and H₂S, respectively. (B) Iron oxidation in samples from Lake La Cruz chemocline, spiked with Fe(II) and DCMU, and incubated under anoxic conditions either in the light or in the dark in a climatic chamber under controlled conditions. (C) Iron oxidation of an enrichment culture from Lake La Cruz chemocline, predominantly consisting of GSB closely related to Chlorobium ferrooxidans, incubated under anoxic Fe(II)-amended conditions either in the light or in the dark. Modified from Walter et al. (2014)

FIGURE 5

Model of the iron cycle in Lake La Cruz. Integration of the iron biogeochemical cycle with the oxygen and the sulfur cycle. Below the epilimnion and metalimnion (1), the chemocline compartment (2) could be an analog to a Neoarchean ferruginous open ocean. However, as neither the deep monimolimnion nor the sediment compartment (3) demonstrate any Fe(III) accumulation it could also be an analog to the euxinic ocean margins characterizing the Neoarchean ocean. All processes from compartment (2) are established along the chemocline. The boundary between compartment (2) and (3) is conceptual and would be situated few centimeters above the sediment. Regular lines indicate biological processes, curved arrows illustrate diffusion/sedimentation processes and broken lines represent chemical processes. The Sediment compartment accumulates sulfur compounds as FeS_am. (OP) stands for oxygenic phototrophs; (IONR) stands for Fe(II)-oxidizing nitrate-reducing chemotrophs; (DIR) stands for dissimilatory Fe(III)-reducing organotrophs; (IOP) stands for Fe(II)-oxidizing phototrophs; (DSR) stands for dissimilatory sulfate reducing organotrophs; (SOP) stands for sulfide oxidizing phototrophs; and (Met) stands for methanogens.