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Primary Endosymbiosis and the Evolution of Light and Oxygen Sensing in Photosynthetic Eukaryotes

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Primary Endosymbiosis and the Evolution of Light and Oxygen Sensing in Photosynthetic Eukaryotes

Nathan C Rockwell et al. Front Ecol Evol.

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.

Keywords: Archaeplastida; algal evolution; ferredoxin-depending bilin reductase; phagotrophy; phytochrome; primary endosymbiosis.

Figures

Figure 1
Figure 1
Endosymbiotic origin of the Archaeplastida plastid through cyanobacterial primary endosymbiosis. (top) A heterotrophic protist engulfed free-living cyanobacteria for food (phagocytosis). Over time, this situation changed, with the cyanobacterium becoming an endosymbiont (bottom). A chlamydial cell is believed to have also been resident in the host at the time of endosymbiosis and provided functions critical to plastid integration (Ball et al., 2013). Both of these prokaryotes gave rise to nuclear genes in the Archaeplastida host through endosymbiotic gene transfer (EGT; cyanobacterium) and horizontal gene transfer (HGT; chlamydial cell and other bacteria). After their split, the red and green algae gave rise to the plastid in other algae through independent secondary endosymbiosis (Bhattacharya et al., 2004; Curtis et al., 2012). The intracellular transfer of genes via EGT and HGT is indicated (arrows). Genetic material of foreign origin in the nucleus is shown as stripes of different colors with the color indicating the source of the gene.
Figure 2
Figure 2
A chlamydial or proteobacterial origin for plastid hexose-phosphate transporters. Maximum likelihood (PhyML) phylogeny of UhpC-type hexose-phosphate transporters in algae, plants, and bacteria (for details, see Price et al., 2012). Bootstrap values (when ≥50%) are shown at the branches. Red algae, Viridiplantae, glaucophytes, and Chlamydiae are shown in red, green, magenta, and blue text, respectively.
Figure 3
Figure 3
Biosynthesis of bilins. A common tetrapyrrole pathway gives rise to both heme and chlorophyll (top). Breakdown of heme proceeds via action of a heme oxygenase (HO) and a ferredoxin-dependent bilin reductase (FDBR). Different FDBRs carry out the same reaction (reduction) on different parts of the tetrapyrrole (bottom). This difference in regiospecificities allows production of a range of bilins with different spectral properties from a single precursor.
Figure 4
Figure 4
Distribution of phytochromes and FDBRs in eukaryotic algae. Evolution of primary algae (Archaeplastidae) is shown, with glaucophyte (blue), rhodophyte (red) and Viridiplantae (green) lineages. We define subsequent evolution of the Viridiplantae with an initial split into streptophytes and prasinophytes. The streptophytes comprise modern charophytes and land plants (embryophytes). Modern charophyte and prasinophyte algae are paraphyletic, with land plants and chlorophyte algae descending from charophytes and prasinophytes, respectively (Worden et al., 2009; Timme et al., 2012; Duanmu et al., 2014). Subsequent endosymbioses (dashed grey arrows) gave rise to secondary algae (parentheses), which are color-coded to indicate the Archaeplastida lineage that was assimilated. Tertiary endosymbioses of diatoms by dinoflagellates are not shown. Distribution of phytochromes was assessed by performing BLAST searches of genomic and transcriptomic data (with default parameters) using the cyanobacterial phytochrome Cph1 as a query sequence. The presence of FDBRs was assessed using a similar strategy, with PcyA from Anabaena sp. strain PCC 7120 and PebA and PebB from Nostoc punctiforme as query sequences. FDBRs were assigned to the PcyA, PebA, or PebB lineage based on BLAST scores with the three query sequences, an approach that provided both unambiguous assignment of algal FDBRs and recovery of the three lineages detected previously (Chen et al., 2012). The presence of PcyA only in certain divisions within rhodophytes and cryptophytes is indicated by the asterisk (e.g., presence of PcyA in the cryptophyte genus Hemiselmis). Question marks indicate groups for which complete draft genomes and/or >3 transcriptomic datasets are not yet available.
Figure 5
Figure 5
Perception of light by phytochrome. (A) Absorption of light by phytochrome triggers reversible photoisomerization of the bilin 15,16-double bond, resulting in photoconversion between two photostates. Rings and numbering system are indicated for a covalent PCB adduct to a conserved Cys residue. Et, ethyl; P, propionate. (B) In land plants, the two photostates absorb red (15Z configuration, blue) and far-red (15E configuration, orange) light. (C) Phytochromes from eukaryotic algae exhibit much more diverse photoperception.

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