Identification of Two Homologous Genes, chlA and chlA, That Are Differentially Involved in Isocyclic Ring Formation of Chlorophyll a in the Cyanobacterium Synechocystis sp. PCC 6803

Minamizaki, Kei; Mizoguchi, Tadashi; Goto, Takeaki; Tamiaki, Hitoshi; Fujita, Yuichi

doi:10.1074/jbc.m708954200

Cited by 72 publications

(89 citation statements)

References 39 publications

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“…and chlorophyll a biosynthesis under low-oxygen conditions (Minamizaki et al, 2008). In addition, we observed upregulation of chlG (slr0056), encoding chlorophyll a synthase and downregulation of chlN (slr0750) and por (slr0506) in both strains (Table 2).…”

Section: The Absence Of Hik31 Alters Transcriptional Response To Low mentioning

confidence: 59%

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

2011

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We have investigated the response of the cyanobacterium Synechocystis sp. PCC 6803 during growth at very low O 2 concentration (bubbled with 99.9 % N 2 /0.1 % CO 2 ). Significant transcriptional changes upon low-O 2 incubation included upregulation of a cluster of genes that contained psbA1 and an operon that includes a gene encoding the two-component regulatory histidine kinase, Hik31. This regulatory cluster is of particular interest, since there are virtually identical copies on both the chromosome and plasmid pSYSX. We used a knockout mutant lacking the chromosomal copy of hik31 and studied differential transcription during the aerobiclow-O 2 transition in this DHik31 strain and the wild-type. We observed two distinct responses to this transition, one Hik31 dependent, the other Hik31 independent. The Hik31-independent responses included the psbA1 induction and genes involved in chlorophyll biosynthesis. In addition, there were changes in a number of genes that may be involved in assembling or stabilizing photosystem (PS)II, and the hox operon and the LexA-like protein (Sll1626) were upregulated during low-O 2 growth. This family of responses mostly focused on PSII and overall redox control. There was also a large set of genes that responded differently in the absence of the chromosomal Hik31. In the vast majority of these cases, Hik31 functioned as a repressor and transcription was enhanced when Hik31 was deleted. Genes in this category encoded both core and peripheral proteins for PSI and PSII, the main phycobilisome proteins, chaperones, the ATP synthase cluster and virtually all of the ribosomal proteins. These findings, coupled with the fact that DHik31 grew better than the wild-type under low-O 2 conditions, suggested that Hik31 helps to regulate growth and overall cellular homeostasis. We detected changes in the transcription of other regulatory genes that may compensate for the loss of Hik31. We conclude that Hik31 regulates an important series of genes that relate to energy production and growth and that help to determine how Synechocystis responds to changes in O 2 conditions.

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Section: The Absence Of Hik31 Alters Transcriptional Response To Low mentioning

confidence: 59%

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

2011

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“…In the case of Synechocystis Δycf54, it may be that the small amount of Chl a produced by this strain is due to the presence of three orthologs of bchE in the genome of this organism. It once was believed that proteins encoded by these genes did not contribute to Chl biosynthesis (13); however, the recent finding that cyanobacterial bchE orthologs from two strains of Cyanothece restore BChl a biosynthesis in a bchE mutant of Rba. capsulatus demonstrates the activity of O 2 -independent BchE orthologs from oxygenic phototrophs (29).…”

Section: Discussionmentioning

confidence: 99%

“…Before the present study, only AcsF had been identified as a bona fide cyclase subunit (8,13). Ycf54 and its ortholog LCAA were subsequently discovered to be required for the normal activity of cyanobacterial and plant enzymes, respectively (21, 22), but the absence of genes encoding Ycf54 from acsF-containing anoxygenic bacterial phototrophs suggested that it might not be a catalytic subunit.…”

Section: Discussionmentioning

confidence: 99%

“…gelatinosus contains both BchE and AcsF cyclases, conferring the ability to synthesize BChl under varying O 2 regimes (9). Orthologs of acsF are widely distributed in phototrophs and have been studied in higher plants (10,11), algae (12) and cyanobacteria (13), the green nonsulfur bacterium Chloroflexus aurantiacus (14), and the purple alphaproteobacterium Rhodobacter (Rba.) sphaeroides (15) (Fig.…”

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confidence: 99%

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Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Chen

Canniffe

Hunter

2017

Proc. Natl. Acad. Sci. U.S.A.

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The biosynthesis of (bacterio)chlorophyll pigments is among the most productive biological pathways on Earth. Photosynthesis relies on these modified tetrapyrroles for the capture of solar radiation and its conversion to chemical energy. (Bacterio)chlorophylls have an isocyclic fifth ring, the formation of which has remained enigmatic for more than 60 y. This reaction is catalyzed by two unrelated cyclase enzymes using different chemistries. The majority of anoxygenic phototrophic bacteria use BchE, an O 2 -sensitive [4Fe-4S] cluster protein, whereas plants, cyanobacteria, and some phototrophic bacteria possess an O 2 -dependent enzyme, the major catalytic component of which is a diiron protein, AcsF. Plant and cyanobacterial mutants in ycf54 display impaired function of the O 2 -dependent enzyme, accumulating the reaction substrate. Swapping cyclases between cyanobacteria and purple phototrophic bacteria reveals three classes of the O 2 -dependent enzyme. AcsF from the purple betaproteobacterium Rubrivivax (Rvi.) gelatinosus rescues the loss not only of its cyanobacterial ortholog, cycI, in Synechocystis sp. PCC 6803, but also of ycf54; conversely, coexpression of cyanobacterial cycI and ycf54 is required to complement the loss of acsF in Rvi. gelatinosus. These results indicate that Ycf54 is a cyclase subunit in oxygenic phototrophs, and that different classes of the enzyme exist based on their requirement for an additional subunit. AcsF is the cyclase in Rvi. gelatinosus, whereas alphaproteobacterial cyclases require a newly discovered protein that we term BciE, encoded by a gene conserved in these organisms. These data delineate three classes of O 2 -dependent cyclase in chlorophototrophic organisms from higher plants to bacteria, and their evolution is discussed herein.

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“…AcsF homologs have since been identified in many photosynthetic eukaryotes including C. reinhardtii (18), Arabidopsis thaliana (19), and barley (15). Two acsF-like genes, sll1214 and sll1874, have been identified in Synechocystis PCC 6803 (hereafter Synechocystis) (20); Sll1214 is essential for growth under aerobic conditions (20) and, to a certain extent, micro-oxic conditions (21), whereas Sll1874 was found to be essential for growth in micro-oxic conditions (20,21).…”

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confidence: 99%

Conserved Chloroplast Open-reading Frame ycf54 Is Required for Activity of the Magnesium Protoporphyrin Monomethylester Oxidative Cyclase in Synechocystis PCC 6803

Hollingshead

Kopečná

Jackson

et al. 2012

Journal of Biological Chemistry

109

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Identification of Two Homologous Genes, chlA and chlA, That Are Differentially Involved in Isocyclic Ring Formation of Chlorophyll a in the Cyanobacterium Synechocystis sp. PCC 6803

Cited by 72 publications

References 39 publications

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Conserved Chloroplast Open-reading Frame ycf54 Is Required for Activity of the Magnesium Protoporphyrin Monomethylester Oxidative Cyclase in Synechocystis PCC 6803

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