Evolutionary Aspects and Regulation of Tetrapyrrole Biosynthesis in Cyanobacteria under Aerobic and Anaerobic Environments

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.

A Novel Structural and Functional Insight Into Chloroplast-Encoded Central Subunit of Dark-Operated Protochlorophyllide Oxidoreductase (Dpor) of Plants

“…Different studies have been carried out to reveal the roles of DPOR subunits. A number of independent studies have revealed that ChlB is essentially important compared to other two subunits (ChlL and ChlN) for light independent protochlorophyllide reduction, hence could be engineered to improve photosynthesis (Karpinska et al, 1997;Cahoon and Timko, 2000;Fujita et al, 2015). But the complete structural and functional annotation of ChlB subunit is yet to be elaborated.…”

“…To date, the sequenced plastid genomes have revealed that plastomes either encode all three subunits or completely lack these genes. Nevertheless, it has been observed experimentally that ChlB is most essential as compared to other subunits encoded by ChlL and ChlN genes for light independent protochlorophyllide reduction in chlorophyll biosynthesis (Karpinska et al, 1997;Cahoon and Timko, 2000;Fujita et al, 2015). Disruption of the ChlB gene from plastome of Chlamydomonas reinhardtii developed yellow mutants (Liu et al, 1993), whereas null mutants of cyanobacterium failed to synthesize chlorophyll under dark conditions .…”

Identification of the chlE gene encoding oxygen-independent Mg-protoporphyrin IX monomethyl ester cyclase in cyanobacteria

“…1). There are two evolutionarily unrelated MPE cyclases in photosynthetic organisms [1,2]. One is an oxygen-independent MPE cyclase, BchE, named after the gene bchE of Rhodobacter capsulatus [3].…”

Isolation of cyanobacterial mutants exhibiting growth defects under microoxic conditions by transposon tagging mutagenesis of <i>Synechocystis</i> sp. PCC 6803

“…While some species might have become extinct because of the production of reactive oxygen species derived from oxygen, in addition to the inactivation of various iron-sulfur enzymes, some organisms might have reconstructed their metabolic processes in response to the aerobic environment to survive. For example, in Chl biosynthesis the iron-sulfur enzyme, dark-operative protochlorophyllide reductase (DPOR), may be inactivated by oxygen, and then a new enzyme, light-dependent protochlorophyllide reductase (LPOR), may be generated (Fujita et al, 2015;Yamazaki et al, 2006). In this case, inactivation of an iron-sulfur enzyme (DPOR) by oxygen causes the generation of a new enzyme (LPOR).…”

“…Chlorophyll (Chl) a is a tetrapyrrole pigment essential for photosynthesis, and the production of Chl a requires oxygen for some biosynthetic reactions. Cyanobacteria possess a gene set encoding biosynthetic enzymes that work specifically under low-oxygen conditions (Aoki et al, 2011;Fujita et al, 2015;Goto et al, 2010;Minamizaki et al, 2008). Once cells are exposed to hypoxia, the gene set for low-oxygen-type enzymes is induced to complement the production of Chl a under low-oxygen conditions.…”