Abstract
Evidence for Fe(II) oxidation and deposition of Fe(III)-bearing minerals from anoxic or redox-stratified Precambrian oceans has received support from decades of sedimentological and geochemical investigation of Banded Iron Formations (BIF). While the exact mechanisms of Fe(II) oxidation remains equivocal, reaction with O2 in the marine water column, produced by cyanobacteria or early oxygenic phototrophs, was likely. In order to understand the role of cyanobacteria in the deposition of Fe(III) minerals to BIF, we must first know how planktonic marine cyanobacteria respond to ferruginous (anoxic and Fe(II)-rich) waters in terms of growth, Fe uptake and homeostasis, and Fe mineral formation. We therefore grew the common marine cyanobacterium Synechococcus PCC 7002 in closed bottles that began anoxic, and contained Fe(II) concentrations that span the range of possible concentrations in Precambrian seawater. These results, along with cell suspension experiments, indicate that Fe(II) is likely oxidized by this strain via chemical oxidation with oxygen produced during photosynthesis, and not via any direct enzymatic or photosynthetic pathway. Imaging of the cell-mineral aggregates with scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM) are consistent with extracellular precipitation of Fe(III) (oxyhydr)oxide minerals, but that >10% of Fe(III) sorbs to cell surfaces rather than precipitating. Proteomic experiments support the role of reactive oxygen species (ROS) in Fe(II) toxicity to Synechococcus PCC 7002. The proteome expressed under low Fe conditions included multiple siderophore biosynthesis and siderophore and Fe transporter proteins, but most siderophores are not expressed during growth with Fe(II). These results provide a mechanistic and quantitative framework for evaluating the geochemical consequences of perhaps life’s greatest metabolic innovation, i.e. the evolution and activity of oxygenic photosynthesis, in ferruginous Precambrian oceans.
Highlights
Iron (Fe) is an essential element to all life, but its bioavailability in aqueous environments has shifted throughout Earth’s history, primarily in response to the oxidation of surface waters
The higher abundances of Fe(II) in the oceans during Precambrian time necessitate an understanding of how cyanobacteria respond to elevated Fe(II) in terms of growth and oxygen production
Our growth experiments with Synechococcus PCC 7002 under initially anoxic, Fe(II)-rich conditions demonstrate that toxicity associated with oxygen production in the presence of Fe is a response to Fe(II), but not to Fe(III)
Summary
Iron (Fe) is an essential element to all life, but its bioavailability in aqueous environments has shifted throughout Earth’s history, primarily in response to the oxidation of surface waters. During the Precambrian Eon [4.6 billion years (Gy) ago to 541 million years (My) ago], anoxic and ferruginous oceans were a persistent feature of Earth’s surface (Canfield, 1998; Planavsky et al, 2011; Poulton and Canfield, 2011), where Fe(II) concentrations in the deep oceans are estimated to have been between 40 and 120 μM (Canfield, 2005). Because of pervasive surface oxidation, fewer modern environments exist today in which ferruginous waters [i.e., containing free Fe(II)] enter sunlit, circumneutral pH environments. We have little physiological context for understanding the activity of cyanobacteria under ferruginous conditions, yet this is crucial for evaluating their activity in Precambrian oceans
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