Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes

Abstract

The origin of the photosynthetic organelle in eukaryotes, the plastid, changed forever the evolutionary trajectory of life on our planet. Plastids are highly specialized compartments derived from a putative single cyanobacterial primary endosymbiosis that occurred in the common ancestor of the supergroup Archaeplastida that comprises the Viridiplantae (green algae and plants), red algae, and glaucophyte algae. These lineages include critical primary producers of freshwater and terrestrial ecosystems, progenitors of which provided plastids through secondary endosymbiosis to other algae such as diatoms and dinoflagellates that are critical to marine ecosystems. Despite its broad importance and the success of algal and plant lineages, the phagotrophic origin of the plastid imposed an interesting challenge on the predatory eukaryotic ancestor of the Archaeplastida. By engulfing an oxygenic photosynthetic cell, the host lineage imposed an oxidative stress upon itself in the presence of light. Adaptations to meet this challenge were thus likely to have occurred early on during the transition from a predatory phagotroph to an obligate phototroph (or mixotroph). Modern algae have recently been shown to employ linear tetrapyrroles (bilins) to respond to oxidative stress under high light. Here we explore the early events in plastid evolution and the possible ancient roles of bilins in responding to light and oxygen.

Diatom Phytochromes Reveal the Existence of Far-Red-Light-Based Sensing in the Ocean

“…Putative bilin reductase encoding genes (pebA and pebB-like genes) that could catalyze a further reduction of BV were also found (Supplemental Data Set 2). Nevertheless, they putatively encode enzymes more closely related to phycoerythrobilin (PEB) synthesis than to ferredoxin-dependent bilin reductases, which convert BV to phytochromobilin (PFB) in cyanobacteria and plants, respectively (Rockwell et al, 2014a). We therefore tested the possible binding of different chromophores by expressing Pt-DPH-PSM with ho1 in E. coli along with the Arabidopsis thaliana HY2 or Synechococcus pebA-pebB bilin reductase genes producing PFB and PEB, respectively.…”

“…We hypothesize that perception of low light levels might be favored by the binding of BV by DPH. Other eukaryotic PHYs in oxygenic phototrophs use more reduced bilin chromophores that shift their absorption properties toward shorter wavelengths (Rockwell et al, 2014a). The displacement of the DPH absorption spectrum toward FR wavebands, beyond the spectral window of photosynthetic pigments, (A) Phylogenetic analysis of PHY protein superfamily using the GAF-PHY region.…”

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

“…Owing to the rate-limiting release of BV product, high-throughput HMOX turnover requires a coupled reaction for efficient heme detoxification. This is generally accomplished by bilirubin-generating NADPH-dependent biliverdin reductases in animals and by phytobilin-generating ferredoxin-dependent bilin reductases (FDBRs) in cyanobacteria and photosynthetic eukaryotes (Frankenberg and Lagarias, 2003;Rockwell et al, 2014). FDBRs and HMOXs are localized in plastids, consistent with their roles in synthesizing phycobiliprotein antennae and phytochrome chromophores (Frankenberg-Dinkel and Terry, 2009).…”

Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?

“…A homolog of uhpC was found by Price et al in the genome of C. paradoxa [64], and Facchinelli et al describe the presence of the UhpC protein in the muroplast of this species [62]. The phylogeny of this gene, available in reference [65], shows that it is present in the genome of glaucophytes, red algae and green algae and that it was probably acquired by HGT from Chlamydiae in the common ancestor of Archaeplastida. All these observations, together with the absence of phosphate transporters of the NST family in Cyanophora, prompted Facchinelli et al [62] to speculate that UphC may have been the first protein used to export carbon from the cyanobiont, making it directly available for glycogen synthesis in the host.…”