A physiological perspective on the origin and evolution of photosynthesis

Abstract

The origin and early evolution of photosynthesis are reviewed from an ecophysiological perspective. Earth's first ecosystems were chemotrophic, fueled by geological H2 at hydrothermal vents and, required flavin-based electron bifurcation to reduce ferredoxin for CO2 fixation. Chlorophyll-based phototrophy (chlorophototrophy) allowed autotrophs to generate reduced ferredoxin without electron bifurcation, providing them access to reductants other than H2. Because high-intensity, short-wavelength electromagnetic radiation at Earth's surface would have been damaging for the first chlorophyll (Chl)-containing cells, photosynthesis probably arose at hydrothermal vents under low-intensity, long-wavelength geothermal light. The first photochemically active pigments were possibly Zn-tetrapyrroles. We suggest that (i) after the evolution of red-absorbing Chl-like pigments, the first light-driven electron transport chains reduced ferredoxin via a type-1 reaction center (RC) progenitor with electrons from H2S; (ii) photothioautotrophy, first with one RC and then with two, was the bridge between H2-dependent chemolithoautotrophy and water-splitting photosynthesis; (iii) photothiotrophy sustained primary production in the photic zone of Archean oceans; (iv) photosynthesis arose in an anoxygenic cyanobacterial progenitor; (v) Chl a is the ancestral Chl; and (vi), anoxygenic chlorophototrophic lineages characterized so far acquired, by horizontal gene transfer, RCs and Chl biosynthesis with or without autotrophy, from the architects of chlorophototrophy-the cyanobacterial lineage.

Figure 1.

Midpoint potentials of some redox couples relevant to this paper. The relevant redox couples for chemolithoautotrophic primary production are the uppermost three. Values are from Thauer, Jungermann and Decker (1977), Brune (1989), Griffin, Schott and Schink (2007), Sharma et al. (2012) and Lengeler, Drews and Schlegel (1999). The H₂AsO₄/H₃AsO₃ couple (arsenate/arsenite, not shown) has a midpoint potential at pH 7 of +54 mV and is used by some chlorophototrophic proteobacteria (Budinoff and Hollibaugh 2008).

Figure 2.

A proposal for the origin of Chl-based phototrophy (see the text). In the primitive, ancestral pathway, a side activity of ferrochelatase produces Zn-PPIX as in modern cells although Zn²⁺ can also spontaneously insert into PPIX. Zn-PPIX could bind to an abundant soluble heme-binding protein, leading to a photoactive protein that could have reduced soluble Fd and replaced flavin-based electron bifurcation. Williamson et al. (2011) have discussed the possible role of Zn-tetrapryrroles as functional intermediates in Chl evolution.

Figure 3.

Structural changes and enzymes needed to convert PPIX into chlorophyllide a. Modified from Bryant and Liu (2013). PPIX with the changes that generate Zn-Proto IX (left) and chlorophyllide a (right). Zn-PPIX is photochemically active and accumulates in Mg-chelatase mutatants of R. sphaeroides through a side activity of ferrochelatase (Jaschke et al.2011). Chloracidobacterium thermophilum uses Zn-BChl a^΄ in its RC (Tsukatani et al.2012). BciD (not shown in the figure) and BchE are both radical SAM enzymes. BciD catalyzes a 4-electron oxidation of the methyl group at C7 to generate a formyl group. A 4-electron oxidation also occurs during the second part of the BchE reaction, part one being the oxidative ring closure (which is possibly similar to coproporphyrinogen III oxidase), part two being the oxidation to produce the keto group of the isocyclic ring E. See the text.

Figure 4.

Photothiotrophy in the evolution of two photosystems. SQR: sulfide:quinone oxidoreductase. CIII: complex III-like cytochrome complex. Q: quinone. qRC1d, a quinone-reducing RC1 duplicate. X: Sulfite-generating protein. Cyt x: hypothetical carrier (probably a cytochrome). See the text.

Figure 5.

The possible role of photothiotrophy in Earth's history. (A) Redox potentials of reductants for primary production vs time. Midpoint potentials are taken from sources listed in the legend of Fig. 1. GOE: great oxidation event. MIFs: mass-independent sulfur fractionations (a proxy for O₂ absence or presence under 10⁻⁵ present atmospheric levels in the atmosphere). Mass-dependent sulfur isotope effects are also pronounced prior to the GOE (not shown, see the text). Whiffs indicate the presence of oxidants in the water column or slight O₂ presence prior to the GOE. BIFs: banded iron formations. The column ‘primary production’ at right underscores the point that before the origin of chlorophototrophy, primary production was H₂-dependent and mechanistically dependent on flavin-based electron bifurcation (indicated by gray shading). The figure suggests that photothiotrophy preceded photoferrotrophy and water splitting in evolution. (B) A possible photothiotrophic sulfur cycle in Archean oceans before the GOE. See the text.

Figure 6.

Export hypothesis for the distribution of RCs among oxygenic and anoxygenic chlorophototrophs. Ribosomal lineages are indicated with gray lines; transfer of RCs into recipient lineages are indicated with green arrows. OEC: oxygen evolving complex. The origin of plastids (Sanchez-Barraclado et al.2017), where cyanobacteria donated both RC1 and RC2 plus the genes for autotrophy to eukaryotes (Ku et al.2015), is symbolically indicated as a wide arrow branching within the cyanobacterial radiation. The figure makes no statement about the timing of export transfer events relative to the origin of the OEC (probably at or near the time of the GOE) or relative to other transfers. Assuming that a cyanobacterial progenitor invented chlorophototrophy, and that geochemical evidence for ancient phototrophy at around 3.2 to 3.4 Ga before present represents photothiotrophy, then photothiotrophy would trace to that age. The photothiotrophic cyanobacterial lineage existent prior to the origin of the OEC corresponds to protocyanobacteria in our terminology here. Note that we indicate no ribosomal lineage branching patterns at all (except plastids), including Melainabacteria or Sericytochromatia relative to cyanobacteria, because ancient lineage relationships and branching patterns inevitably change as new phylogenetic methods are employed and as new lineages become known (Williams et al.2013). Symbols for hydrothermal light at photosynthesis and RC1 origin and sunlight at RC2 origin are indicated. See the text.