Phylogenetic Analysis of Sulfate Assimilation and Cysteine Biosynthesis in Phototrophic Organisms

Abstract

Sulfur is an essential nutrient for all organisms. The majority of sulfur in nature is found in inorganic form of sulfate, which has to be reduced and incorporated into bioorganic compounds. Assimilatory sulfate reduction occurs in various chemotrophic bacteria and fungi and in photosynthetic organisms, but is missing in animals and most prokaryotic and eukaryotic obligate parasites. Despite its central position in plant primary metabolism, the question of evolution of the pathway and origin of plant genes involved in sulfate assimilation has never been addressed. We have therefore made use of the vast amount of available sequence data to perform a phylogenetic analysis of sulfate assimilation genes from a range of lineages of photosynthetic organisms including photosynthetic bacteria, primary symbionts such as plants, green and red algae and various secondary and tertiary symbionts. The analysis revealed very complicated relations between the different lineages and different evolutionary histories of the individual genes of the pathway. Whereas, for example, plant sulfite reductase is clearly of a cyanobacterial origin, the other genes in the pathway, although being plastidial are, unusually, not of cyanobacterial origin. The clear separation between adenosine phosphosulfate- and phosphoadenosine phosphosulfate-reducing organisms seen in previous analyses has been lost with the inclusion of genes from diatom and cryptomonad secondary symbiont algae. In fact, a new variant of the key enzyme of sulfate assimilation, adenosine 5'-phosphosulfate reductase, lacking an iron sulfur cofactor, has been discovered. In addition, many interesting fusion proteins between various components of the pathway were uncovered in the newly sequenced algal genomes which open new exciting opportunities to improve the efficiency of the pathway or some of its reactions. In the chapter, protein phylogenies of seven enzymes of the pathway will be discussed in detail with relation to distribution of enzyme variants among prokaryotic and eukaryotic lineages, origin of plant genes, and the origin of genes in algae with secondary and tertiary plastids.