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

Yamanashi, Kaori; Minamizaki, Kei; Fujita, Yuichi

doi:10.1016/j.bbrc.2015.06.124

Cited by 16 publications

(11 citation statements)

References 31 publications

(36 reference statements)

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“…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%

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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Section: Discussionmentioning

confidence: 99%

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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“…There is also an O2-independent cyclase, BchE, which incorporates oxygen donated from water (196). Although BchE homologs (termed ChlE) have been found in some cyanobacteria (197), the O2independent cyclase is found mainly in anoxygenic phototrophic bacteria, and it will be described in the bacteriochlorophyll (BChl) section below. Pinta et al (198) assigned AcsF (aerobic cyclization system Fe-containing subunit) in the purple betaproteobacterium Rubrivivax gelatinosus to the O2-dependent reaction, and homologs were subsequently found in all oxygenic photosynthetic organisms investigated.…”

Section: The Transformation Of Protoix Into Chls -Chl Amentioning

confidence: 99%

Biosynthesis of the modified tetrapyrroles—the pigments of life

Bryant

Hunter

Warren

2020

Journal of Biological Chemistry

175

164

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Modified tetrapyrroles are large macrocyclic compounds, consisting of diverse conjugation and metal chelation systems and imparting an array of colors to the biological structures that contain them. Tetrapyrroles represent some of the most complex small molecules synthesized by cells and are involved in many essential processes that are fundamental to life on Earth, including photosynthesis, respiration, and catalysis. These molecules are all derived from a common template through a series of enzyme-mediated transformations that alter the oxidation state of the macrocycle and also modify its size, its side-chain composition, and the nature of the centrally chelated metal ion. The different modified tetrapyrroles include chlorophylls, hemes, siroheme, corrins (including vitamin B12), coenzyme F430, heme d1, and bilins. After nearly a century of study, almost all of the more than 90 different enzymes that synthesize this family of compounds are now known, and expression of reconstructed operons in heterologous hosts has confirmed that most pathways are complete. Aside from the highly diverse nature of the chemical reactions catalyzed, an interesting aspect of comparative biochemistry is to see how different enzymes and even entire pathways have evolved to perform alternative chemical reactions to produce the same end products in the presence and absence of oxygen. Although there is still much to learn, our current understanding of tetrapyrrole biogenesis represents a remarkable biochemical milestone that is summarized in this review.

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“…1). Firstly, there are two evolutionarily distinct types of Mg-protoporphyrin IX monomethyl ester cyclase (MgPME cyclase), one is a multi-subunit enzyme (Yamanashi et al, 2015;Chen et al, 2017) and the other is a single-subunit enzyme encoded by chlE (Yamanashi et al, 2015). To our knowledge, neither of the enzymes has been detected in complex algae (e.g., diatoms;Wilhelm et al 2006;Nymark et al 2009).…”

Section: Chlorophorummentioning

confidence: 99%

Peer Review #2 of "Patterns in evolutionary origins of heme, chlorophyll a and isopentenyl diphosphate biosynthetic pathways suggest non-photosynthetic periods prior to plastid replacements in dinoflagellates (v0.2)"

Dorrell¹

2018

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Background: The ancestral dinoflagellate most likely established a peridinin-containing plastid, which have been inherited to the extant photosynthetic descendants. However, kareniacean dinoflagellates and Lepidodinium species were known to bear "non-canonical" plastids lacking peridinin, which were established through haptophyte and a green algal endosymbioses, respectively. For plastid function and maintenance, the aforementioned dinoflagellates were known to use nucleus-encoded proteins vertically inherited from the ancestral dinoflagellates (vertically inherited-or VI-type), and those acquired from non-dinoflagellate organisms (including the endosymbiont). These observations indicated that the proteomes of the non-canonical plastids derived from a haptophyte and a green alga were modified by "exogenous" genes acquired from non-dinoflagellate organisms. However, there was no systematic evaluation addressing how "exogenous" genes reshaped individual metabolic pathways localized in a non-canonical plastid. Results: In this study, we surveyed transcriptomic data from two kareniacean species (Karenia brevis and Karlodinium veneficum) and Lepidodinium chlorophorum, and identified proteins involved in three plastid metabolic pathways synthesizing chlorophyll a (Chl a), heme and isoprene. The origins of the individual proteins of our interest were investigated, and assessed how the three pathways were modified before and after the algal endosymbioses, which gave rise to the current non-canonical plastids. We observed a clear difference in the contribution of VI-type proteins across the three pathways. In both Karenia/Karlodinium and Lepidodinium, we observed a substantial contribution of VI-type proteins to the isoprene and heme biosynthesises. In sharp contrast, VI-type protein was barely detected in the Chl a biosynthesis in the three dinoflagellates. Discussion: Pioneering works hypothesized that the ancestral kareniacean species had lost the photosynthetic activity prior to haptophyte endosymbiosis. The absence of VI-type proteins in the Chl a biosynthetic pathway in Karenia or Karlodinium is in good agreement with the putative nonphotosynthetic nature proposed for their ancestor. The dominance of proteins with haptophyte origin in the Karenia/Karlodinium pathway suggests that their ancestor rebuilt the particular pathway by genes acquired from the endosymbiont. Likewise, we here propose that the ancestral Lepidodinium likely experienced a non-photosynthetic period and discarded the entire Chl a biosynthetic pathway prior to the green algal endosymbiosis. Nevertheless, Lepidodinium rebuilt the pathway by genes transferred from phylogenetically diverse organisms, rather than the green algal endosymbiont. We explore the reasons why green algal genes were barely utilized to reconstruct the Lepidodinium pathway.

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

Cited by 16 publications

References 31 publications

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

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

Biosynthesis of the modified tetrapyrroles—the pigments of life

Peer Review #2 of "Patterns in evolutionary origins of heme, chlorophyll a and isopentenyl diphosphate biosynthetic pathways suggest non-photosynthetic periods prior to plastid replacements in dinoflagellates (v0.2)"

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