Nutrient Acquisition and the Metabolic Potential of Photoferrotrophic Chlorobi

Katharine J. Thompson, Rachel L. Simister, Aria S. Hahn, Steven J. Hallam, Sean A. Crowe

Anoxygenic photosynthesis evolved prior to oxygenic photosynthesis and harnessed energy from sunlight to support biomass production on the early Earth. Models that consider the availability of electron donors predict that anoxygenic photosynthesis using Fe(II), known as photoferrotrophy, would have supported most global primary production before the proliferation of oxygenic phototrophs at approximately 2.3 billion years ago. These photoferrotrophs have also been implicated in the deposition of banded iron formations, the world's largest sedimentary iron ore deposits that formed mostly in late Archean and early Proterozoic Eons. In this work we present new data and analyses that illuminate the metabolic capacity of photoferrotrophy in the phylum Chlorobi. Our laboratory growth experiments and biochemical analyses demonstrate that photoferrotrophic Chlorobi are capable of assimilatory sulfate reduction and nitrogen fixation under sulfate and nitrogen limiting conditions, respectively. Furthermore, the evolutionary histories of key enzymes in both sulfur (CysH and CysD) and nitrogen fixation (NifDKH) pathways are convoluted; protein phylogenies, however, suggest that early Chlorobi could have had the capacity to assimilate sulfur and fix nitrogen. We argue, then, that the capacity for photoferrotrophic Chlorobi to acquire these key nutrients enabled them to support primary production and underpin global biogeochemical cycles in the Precambrian.