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.
Highlights
Photosynthesis is the main primary production process fueling life on Earth
Reduced iron [Fe(II)], of hydrothermal origin (Klein, 2005), from biologically processed continental sources (Li et al, 2015), and/or released by tectono-magmatic events (Konhauser et al, 2007a), dominated the mesophilic (Hren et al, 2009; Blake et al, 2010; Poulton and Canfield, 2011), sulfurpoor (Shen et al, 2003; Crowe et al, 2014b) Archean ocean chemistry (Figures 1, 2). From these ferruginous conditions a transition toward a more sulfidic ocean occurred from the late Archean to the Mesoproterozoic (Poulton et al, 2004; Canfield et al, 2008; Reinhard et al, 2009), though sulfide was likely spatially confined to parts of the ocean (Reinhard et al, 2013)
(iv) direct oxidation by microbial processes (Garrels et al, 1973; Hartman, 1984; Li et al, 2011; Posth et al, 2013; Czaja et al, 2013; Chan et al, 2016), mainly iron-oxidation by anoxygenic phototrophs using Fe(II) as electron donor, seems an attractive mechanism for early Banded iron formations (BIF) formation, for the time before oxygenic photosynthesis appeared on Earth (Ehrenreich and Widdel, 1994a; Konhauser et al, 2002, 2005, 2007a,b, 2011; Kappler and Newman, 2004; Kappler et al, 2005; Croal et al, 2009; Fru et al, 2013; Li et al, 2013; Eickhoff et al, 2014; Sun et al, 2015)
Summary
Photosynthesis is the main primary production process fueling life on Earth It requires light as energy source, inorganic carbon to be fixed, and a source of electrons (Hamilton et al, 2016). Very different conditions existed on early Earth (Canfield et al, 2006), as the chemical environment (e.g., the availability of electron acceptors and donors for biogeochemical processes) and, the favored biogeochemical processes, differed in the ancient biosphere from those currently prevailing. Some modern ecosystems (the so-called “analogs,” Burns et al, 2009) still show determinant similar features (i.e., redox conditions, iron and sulfur chemistry) to those predominating on ancient Earth, and offer opportunities to study the processes that sustained microbial life in the primitive biosphere. Photoferrotrophs, which use Fe(II) as an electron donor and light as an energy source for inorganic carbon fixation (Widdel et al, 1993), as well as their biogeochemical role in modern and ancient ferruginous systems, are addressed in this review
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