Thinking Twice about the Evolution of Photosynthesis

Abstract

Sam Granick opened his seminal 1957 paper titled Speculations on the Origins and Evolution of Photosynthesis with the assertion that there is a constant urge in human beings to seek beginnings (I concur). This urge has led to an incessant stream of speculative ideas and debates on the evolution of photosynthesis that started in the first half of the twentieth century and shows no signs of abating. Some of these speculative ideas have become common place, are taken as fact, but find little support. Here I review and scrutinise three widely accepted ideas that underpin the current study of the evolution of photosynthesis: firstly, that the photochemical reaction centres used in anoxygenic photosynthesis are more primitive than those in oxygenic photosynthesis; secondly, that the probability of acquiring photosynthesis via horizontal gene transfer is greater than the loss of photosynthesis; and thirdly, and most importantly, that the origin of anoxygenic photosynthesis predates the origin of oxygenic photosynthesis. I shall attempt to demonstrate that these three ideas are often grounded on incorrect assumptions built on more assumptions with no experimental nor observational support. I hope that this brief review will not only serve as cautionary tale, but also that it will open new avenues of research aimed at disentangling the complex evolution of photosynthesis and its impact on the early history of life and the planet.

Comparative transcriptomic analysis reveals conserved transcriptional programs underpinning organogenesis and reproduction in land plants

“…Most of the gene families were gained in node 1 (34 families, Supplementary Table 8). Leaves have multiple origins in land plants 44,45 , however, the programs for oxygenic photosynthesis originated in ancient organisms 46 . In agreement, before the divergence of land plants, we observed enrichment for functions related to photosynthesis (<N8), and after the divergence of land plants, we detected enrichment for additional functions such as external stimuli response, cytoskeleton organization, phytohormone action, and protein modification (Supplementary Table 9).…”

On the origin of oxygenic photosynthesis and Cyanobacteria

“…It is worth highlighting that the deep divergence of anoxygenic and oxygenic photosystems (marked 2 and 3 in Fig. 1), could have been a response to dealing with oxygen itself (Orf et al, 2018;Cardona, 2019). In other words, the origin of water oxidation to oxygen not only predated the D1 and D2 duplication (marked 4 in Fig.…”

“…It is now argued that the photosystems (marked 1 in Fig. 1) uniquely evolved the ability to perform water oxidation from the beginning and, as the photosystems further specialised, tis led to what we now know as oxygenic photosynthesis (Cardona, 2017;Cardona, 2019;. It is worth highlighting that the efficiency of enzymes carrying out water oxidation has changed and improved, and earlier forms predate the evolution of crown group Cyanobacteria (marked 5 in Figs 1, 3).…”

Photosynthesis on exoplanets and exomoons from reflected light

“…In other words, it is relatively easier to extract electrons from strong reductants such as H 2 and H 2 S. Hence, it is not surprising that microbes reliant on these reductants possess comparatively simpler photosynthetic machinery, i.e., they have only a single photosystem (PSI or PSII). It is commonly supposed that the anoxygenic photosynthesis (with its single photosystem) evolved on Earth earlier than its oxygenic counterpart (which has two photosystems), but the evidence favouring this hypothesis has been challenged as of late (Cardona, 2019).…”

“…they have only a single photosystem (PSI or PSII). It is commonly supposed that the anoxygenic photosynthesis (with its single photosystem) evolved on Earth earlier than its oxygenic counterpart (which has two photosystems), but the evidence favouring this hypothesis has been challenged as of late (Cardona 2019).…”