Abstract
Chlorophyll a (Chl) is a light-absorbing tetrapyrrole pigment that is essential for photosynthesis. The molecule is produced from glutamate via a complex biosynthetic pathway comprised of at least 15 enzymatic steps. The first half of the Chl pathway is shared with heme biosynthesis, and the latter half, called the Mg-branch, is specific to Mg-containing Chl a. Bilin pigments, such as phycocyanobilin, are additionally produced from heme, so these light-harvesting pigments also share many common biosynthetic steps with Chl biosynthesis. Some of these common steps in the biosynthetic pathways of heme, Chl and bilins require molecular oxygen for catalysis, such as oxygen-dependent coproporphyrinogen III oxidase. Cyanobacteria thrive in diverse environments in terms of oxygen levels. To cope with Chl deficiency caused by low-oxygen conditions, cyanobacteria have developed elaborate mechanisms to maintain Chl production, even under microoxic environments. The use of enzymes specialized for low-oxygen conditions, such as oxygen-independent coproporphyrinogen III oxidase, constitutes part of a mechanism adapted to low-oxygen conditions. Another mechanism adaptive to hypoxic conditions is mediated by the transcriptional regulator ChlR that senses low oxygen and subsequently activates the transcription of genes encoding enzymes that work under low-oxygen tension. In diazotrophic cyanobacteria, this multilayered regulation also contributes in Chl biosynthesis by supporting energy production for nitrogen fixation that also requires low-oxygen conditions. We will also discuss the evolutionary implications of cyanobacterial tetrapyrrole biosynthesis and regulation, because low oxygen-type enzymes also appear to be evolutionarily older than oxygen-dependent enzymes.
Highlights
Cyanobacteria are prokaryotes that perform oxygenic photosynthesis
This review summarizes recent progress in emerging mechanisms that regulate the biosynthesis of chlorophyll (Chl), heme and bilin in cyanobacteria and highlights the evolution of metabolism in response to the Great Oxidation Event (GOE) that occurred during the late Proterozoic era
In a search for chlR and bchE, we performed a BLAST search to determine their orthologs in cyanobacteria. ¶ A gene set forming a gene cluster in the genome. § A gene set forming another gene cluster in the chromosomal locus other than the gene cluster shown with ¶. * These ChlRs have four conserved Cys residues (4Cys-type ChlR). d The ability of nitrogen fixation is shown by + and –. e In Anabaena PCC 7120, two genes encoding isoforms of HemF and ChlAII are present in the genome, and only one set of hemF and chlAII is located nearby in the opposite directions. f Because this ChlA homolog shows sequence similarity to both ChlAI and ChlAII by KEGG
Summary
Cyanobacteria are prokaryotes that perform oxygenic photosynthesis. Ancient cyanobacteria are believed to be the direct ancestor of chloroplasts in plants obtained by an endosymbiosis event during the early evolution of life [1]. Purple photosynthetic bacteria switch their growth modes between photosynthesis and respiration in response to the environmental oxygen levels. Extensive studies on the regulatory mechanisms of photosynthesis, including bacteriochlorophyll biosynthesis, have been performed in the purple bacteria, Rhodobacter capsulatus and R. sphaeroides. Several regulatory proteins, such as RegB-RegA, FNR and. Cyanobacteria grow photosynthetically irrespective of aerobic or anaerobic conditions, these bacteria must contain some regulatory mechanism(s) to cope with hypoxic and anaerobic conditions to survive, because various oxygenase reactions would likely be retarded at night because of limited oxygen. Knowledge of cyanobacterial adaptation to low-oxygen conditions is limited, because cyanobacteria are regarded as aerobic organisms because of their ability to produce oxygen through photosynthesis. This review summarizes recent progress in emerging mechanisms that regulate the biosynthesis of chlorophyll (Chl), heme and bilin in cyanobacteria and highlights the evolution of metabolism in response to the Great Oxidation Event (GOE) that occurred during the late Proterozoic era
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