Shiladitya DasSarma, et al., propose that retinal-based phototrophy arose early in the evolution of life on Earth, profoundly impacting the development of photosynthesis and creating implications for the search for life beyond our planet. While the early evolutionary history of phototrophy is largely in the realm of the unknown, the onset of oxygenic photosynthesis in primitive cyanobacteria significantly altered the Earth’s atmosphere by contributing to the rise of oxygen ∼2.3 billion years ago. However, photosynthetic chlorophyll and bacteriochlorophyll pigments lack appreciable absorption at wavelengths about 500–600 nm, an energy-rich region of the solar spectrum. By contrast, simpler retinal-based light-harvesting systems such as the haloarchaeal purple membrane protein bacteriorhodopsin show a strong well-defined peak of absorbance centred at 568 nm, which is complementary to that of chlorophyll pigments.
The authors propose a scenario where simple retinal-based light-harvesting systems like that of the purple chromoprotein bacteriorhodopsin, originally discovered in halophilic Archaea, may have dominated prior to the development of photosynthesis. They explore this hypothesis, termed the ‘Purple Earth,’ and discuss how retinal photopigments may serve as remote biosignatures for exoplanet research.
The major events sparking life on Earth on our 4.6-billion-year-old planet remain enigmatic, although there is general agreement that first life likely arose about 3.7–4.1 billion years ago, during the early Archean or late Hadean eons (Abramov and Mojzsis, 2009; Deamer, 2011; Bell et al., 2015; Knoll, 2015). Evidence for the presence of isoprenoid compounds has been reported in ancient sediments not long after, suggesting the early rise of Archaea (Hahn and Haug, 1986; Ventura et al., 2007). The early rise of Archaea is also suggested by phylogenic studies, although lateral gene transfers have complicated their interpretation (Lange, et al., 2000; Kennedy et al., 2001; Brochier-Armanet et al., 2011; Hoshino and Gaucher, 2018). Stromatolites representing fossilized microbial mats have been estimated to be up to 3.7 billion-years-old (Walter et al., 1980; Vankranendonk et al., 2008; Nutman et al., 2016) and radiocarbon dating has shown 12 C enrichment from this early period, consistent with the development of photosynthetic microorganisms (Ohtomo et al., 2014). There is wide agreement that anoxygenic photosynthesis preceded oxygenic photosynthesis, though the length of the interval for this transition is uncertain (Olson, 2006; Buick, 2008; Rothschild, 2008).
Some geochemical proxy records suggest that the earliest oxygenic photosynthesizers may have appeared by ∼2.9–3 Ga with geochemical sinks arresting oxygen’s accumulation for a time (Nisbet et al., 2007; Planavsky et al., 2014). Ultimately, because of oxygenic photosynthesis and additional, poorly understood factors, the Earth experienced a Great Oxidation Event about 2.3 billion years ago, which indelibly altered the prevailing chemical conditions of our planet’s atmosphere (Kump, 2008; Lyons et al., 2014; Luo et al., 2016).
What were the important evolutionary events predating the rise of photosynthesis during the early history of life on Earth? Although the events during this very early time are not clear, in this paper, we discuss a speculative hypothesis for early evolution, called the ‘Purple Earth,’ which posits the rise of retinal pigment-based phototrophic life forms on Earth’s surface prior to anoxygenic and oxygenic photosynthesis. In this view, retinal pigments may have competed with and affected the evolution of photosynthetic pigments and indeed still complements them today in Earth’s oceans and other environments. Early microorganisms employing retinal pigments for generating metabolic energy may have dominated, as halophilic Archaea do today in hypersaline environments, providing a scenario which may serve to guide our search for detectable biosignatures on other worlds.