Physiological basis of phototrophy

Photosynthesis is one of the most important biological processes for sustaining life on Earth and has transformed Earth over the course of its history. Although crucial for understanding how we got to the Earth we know today, comprehending how phototrophy operated on the early Earth and contributed to global change remains challenging. Study of “molecular fossils” in the rock record has led to key insights into how phototrophs potentially contributed to nutrient cycling on early Earth, but these data alone are insufficient to reconstruct what metabolisms phototrophs were performing and how they evolved over time. As a complement to the rock record, studying information preserved in currently living photosynthetic organisms can give crucial clues to understanding ancient photosynthesis. Beyond well-studied phototroph groups like crown cyanobacteria, diverse bacterial phototrophs are now known that, although challenging to culture in the lab, perform phototrophy using unique mechanisms that can inform our understanding of the evolutionary and metabolic history of phototrophy. Probing the unique phototrophic physiologies of these bacteria may also yield new hints into how photosynthesis functions, with potential applications in biotechnology and green energy.

A major theme of my research is to explore the physiological basis of phototrophy in these lesser-known bacterial phototrophs, with implications for understanding what ancient phototrophs were like and how they contributed to early ecosystems. My work so far has centered on phototrophs that perform a poorly studied metabolism called photoferrotrophy, where bacteria use light energy to oxidize iron as an electron source. Although only a few bacterial isolates are known to perform photoferrotrophy on the modern Earth, it is thought that this process could represent one of the earliest phototrophic metabolisms and that photoferrotrophy potentially became a widespread process in the iron-rich oceans of early Earth. Huge Banded Iron Formations can be found on the modern Earth that are dated to the Archaean Eon (approx. 2.5-3.8 billion years ago) and are full of oxidized iron minerals – could these record the activity of ancient ecosystems, driven in part by photoferrotrophs? By searching for novel bacteria capable of photoferrotrophy on the modern Earth and probing their physiology, I hope to help refine our understanding of the role of photoferrotrophs in Earth’s history.

My work has identified the genomic potential for photoferrotrophy, driven by novel members of the Chlorobia class, in iron-rich Boreal Shield lakes, although we have yet to confirm photoferrotrophy by these organisms in the lab (Tsuji et al., ISME J, 2020; Schiff et al., Sci Rep, 2017). Probing for photoferrotrophs ultimately led us to grow a highly unusual bacterium, named “Candidatus Chlorohelix allophototropha” (Tsuji et al., Nature, 2024), that performs phototrophy using a highly novel clade of Type I photosynthetic reaction center protein and whose disovery has major implications for understanding the evolution of photosynthesis. In future, I plan to examine the physiology and metabolism of “Ca. Chlorohelix allophototropha” in more detail and to further probe the implications of discovery of this unusual strain for the history of photosynthesis on Earth. I’m very excited for our upcoming work in this area.