Chlorophyll Biosynthesis Gene Evolution Indicates Photosystem Gene Duplication, Not Photosystem Merger, at the Origin of Oxygenic Photosynthesis

Abstract

An open question regarding the evolution of photosynthesis is how cyanobacteria came to possess the two reaction center (RC) types, Type I reaction center (RCI) and Type II reaction center (RCII). The two main competing theories in the foreground of current thinking on this issue are that either 1) RCI and RCII are related via lineage divergence among anoxygenic photosynthetic bacteria and became merged in cyanobacteria via an event of large-scale lateral gene transfer (also called "fusion" theories) or 2) the two RC types are related via gene duplication in an ancestral, anoxygenic but protocyanobacterial phototroph that possessed both RC types before making the transition to using water as an electron donor. To distinguish between these possibilities, we studied the evolution of the core (bacterio)chlorophyll biosynthetic pathway from protoporphyrin IX (Proto IX) up to (bacterio)chlorophyllide a. The results show no dichotomy of chlorophyll biosynthesis genes into RCI- and RCII-specific chlorophyll biosynthetic clades, thereby excluding models of fusion at the origin of cyanobacteria and supporting the selective-loss hypothesis. By considering the cofactor demands of the pathway and the source genes from which several steps in chlorophyll biosynthesis are derived, we infer that the cell that first synthesized chlorophyll was a cobalamin-dependent, heme-synthesizing, diazotrophic anaerobe.

Early emergence of the FtsH proteases involved in photosystem II repair

“…This pattern is also observed in Fig. 1 which also contained non-phototrophic representatives of the same phyla and it is consistent with previous phylogenetic (Quaiser et al 2003, Bryant et al 2012, Sousa et al 2013, Greening et al 2015, Cardona 2016a) and phylogenomic (Ciccarelli 2006, Dutilh et al 2008, Wu and Eisen 2008, Ward et al 2009, Jun et al 2010, David and Alm 2011, Rinke et al 2013, Segata et al 2013, Marin et al 2017) studies that have repeatedly confirmed the Acidobacteria as a sister clade of the Proteobacteria, or branching within the Proteobacteria as a sister clade of the deltaproteobacteria. At the same time, the nearness of the Chlorobi to Acidobacteria and Proteobacteira is also consistent with the ChlorobiBacteroidetes-Fibrobacterere supergroup bifurcating prior to the radiation of the Proteobacteria (Wu and Eisen 2008, Jun et al 2010, David and Alm 2011, Segata et al 2013, Marin et al 2017.…”

“…However, recent detailed analysis of the phylogeny of RC proteins indicates that HGT of RCs to an ancestral nonphotosynthetic cyanobacterium from anoxygenic phototrophic bacteria is unlikely (Cardona 2016b); furthermore, the evolution of RC proteins shows that the last common ancestor to all phototrophic bacteria had already evolved Type I and Type II RC proteins from an earlier gene duplication event (Sousa et al 2013, Harel et al 2015. In addition, it has been argued that the evolution of the structural complexity of PSII and the origin of the oxygenevolving manganese cluster can only be explained if both types of RC had been evolving in cooperation since the dawn of photosynthesis and that water oxidation might therefore have occurred at a far earlier stage of evolution that previously thought (Cardona 2016b(Cardona , 2017.…”

“…In contrast, more recent phylogenetic analyses have led to the suggestion that the evolution of Type I and Type II RCs might have occurred in a single organism after a gene duplication event (Mulkidjanian et al 2006, Sousa et al 2013, Harel et al 2015 and, possibly, that Type I and Type II RCs might have then been transferred at various stages of evolution to other types of nonphotosynthetic bacteria through horizontal gene transfer (HGT) (Mulkidjanian et al 2006). Given the fact that the geochemical record of photosynthesis dates back to 3.5 to 3.8 billion years ago, such 'gene duplication' hypotheses raise the possibility that oxygenic photosynthesis might have evolved much earlier than previously thought, perhaps hundreds of millions of years before the Great Oxidation Event (Lyons et al 2014).…”

Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin

“…How they synthesize chlorophyll remains a mystery, given that all known chlorophyll-synthesizing pathways use protoporphyrin as an intermediate. Such cases are exceedingly rare: Of 72 photosynthetic organisms included in this study (23) (Dataset S1), only three species from two major taxonomic groups fall into this category, namely, Heliobacterium modesticaldum of the Grampositive photosynthetic heliobacteria (44,45) and Roseiflexus sp. RS-1 and Roseiflexus castenholzi of green nonsulfur bacteria (46,47).…”

Early Microbial Evolution: The Age of Anaerobes

“…Oxygenic photosynthesis arose from (after) anoxygenic pho-tosynthesis, on that all biologists agree, but whether the two photosystems of cyanobacteria became divergent in one and the same genome or in different genomes is more debated (Hohmann-Marriott and Blankenship 2011), whereby lack of a deep split in chlorophyll biosynthesis that would mirror the deep spilt of the photosystems is lacking (Sousa et al 2013a), suggesting that the two photosystems arose and diverged within the same cell (Allen 2005). The evolution of photosynthetic electron transport chains (with chlorophylls) requires that basic biochemical components like cytochromes and quinones were in place, meaning that respiratory electron transport chains (with heme) preceded photosynthetic electron transport chains (and O 2 ) in evolution.…”