Properties of the Photosynthetic System and DNA of <i>Cyanophora paradoxa</i> Cyanelles

Klein, Sigrid M.; Jaynes, Jesse M.; Kent, Samuel S.; Vernon, Leo P.

doi:10.1104/pp.68.2.407

Cited by 8 publications

(3 citation statements)

References 14 publications

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“…Regardless of the considerable historical attention that glaucophyte plastids have received due to putative ancestral traits shared with free-living cyanobacteria, such as the vestigial peptidoglycan wall between the organelle membranes (Hall and Claus 1963; Pfanzagl et al. 1996; Löffelhardt and Bohnert 2001; Steiner and Löffelhardt 2011) and similar composition of their photosynthetic apparatuses (Klein et al. 1981; Steiner and Löffelhardt 2011; Misumi and Sonoike 2017), their genomes have long been ignored.…”

Section: Introductionmentioning

confidence: 99%

Plastid Genomes from Diverse Glaucophyte Genera Reveal a Largely Conserved Gene Content and Limited Architectural Diversity

Figueroa-Martínez

Jackson

Reyes‐Prieto

2018

Genome Biology and Evolution

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Plastid genome (ptDNA) data of Glaucophyta have been limited for many years to the genus Cyanophora. Here, we sequenced the ptDNAs of Gloeochaete wittrockiana, Cyanoptyche gloeocystis, Glaucocystis incrassata, and Glaucocystis sp. BBH. The reported sequences are the first genome-scale plastid data available for these three poorly studied glaucophyte genera. Although the Glaucophyta plastids appear morphologically “ancestral,” they actually bear derived genomes not radically different from those of red algae or viridiplants. The glaucophyte plastid coding capacity is highly conserved (112 genes shared) and the architecture of the plastid chromosomes is relatively simple. Phylogenomic analyses recovered Glaucophyta as the earliest diverging Archaeplastida lineage, but the position of viridiplants as the first branching group was not rejected by the approximately unbiased test. Pairwise distances estimated from 19 different plastid genes revealed that the highest sequence divergence between glaucophyte genera is frequently higher than distances between species of different classes within red algae or viridiplants. Gene synteny and sequence similarity in the ptDNAs of the two Glaucocystis species analyzed is conserved. However, the ptDNA of Gla. incrassata contains a 7.9-kb insertion not detected in Glaucocystis sp. BBH. The insertion contains ten open reading frames that include four coding regions similar to bacterial serine recombinases (two open reading frames), DNA primases, and peptidoglycan aminohydrolases. These three enzymes, often encoded in bacterial plasmids and bacteriophage genomes, are known to participate in the mobilization and replication of DNA mobile elements. It is therefore plausible that the insertion in Gla. incrassata ptDNA is derived from a DNA mobile element.

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Section: Introductionmentioning

confidence: 99%

Plastid Genomes from Diverse Glaucophyte Genera Reveal a Largely Conserved Gene Content and Limited Architectural Diversity

Figueroa-Martínez

Jackson

Reyes‐Prieto

2018

Genome Biology and Evolution

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“…The methods used for growth of C. paradoxa and for isolation of the cyanelle were those previously described (8). The original culture of Phormidium laminosum (OH1-P), a gift from Dr. Richard Castenholz, was grown as described by Jackson and Castenholz (5).…”

Section: Methodsmentioning

confidence: 99%

Direct Spectrophotometric Measurement of Photosystem I and Photosystem II Activities of Photosynthetic Membrane Preparations from Cyanophora paradoxa, Phormidium laminosum, and Spinach

Vernon¹,

Cardon²

1982

Plant Physiol.

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Vesicles prepared with the French press from membranes of cyanelles of Cyanophora paradoxa retain 02 evolution activity with rates up to 500 micromoles 2,6-dichlorophenolindophenol reduced per hour per milligram chlorophyll. This activity is immediately lost when the vesicles are transferred from the sucrose-phosphate-citrate preparation buffer into dilute phosphate buffer. Similar preparations from Phormidium laminosum, a thermophilic cyanobacterium retain activity under such conditions. Photosystem I activities of both cyanobacterial vesicle preparations were determined by direct spectrophotometric measurement of N,N,N',N'-tetramethyl-p-phenylenediamine photooxidation in the presence of anthraquinone-2-sulfonate. The rates so determined were compared with rates of 02 taken up in the presence of methyl viologen or anthraquinone-2-sulfonate as electron acceptors. The predicted stoichiometry of two was observed for moles of N,N,N',N'-tetramethyl-p-phenylenediamine TMPD is readily reduced by PSII and oxidized by PSI, as shown by the fact that it overcomes DBMIB inhibition of NADP photoreduction coupled to water oxidation (12). In this case, it serves as a bypass for electron flow past the DBMIB inhibition site. In spinach chloroplasts, TMPD reacts with plastocyanin, which serves as a direct donor to PSI (3). In this study we report on the PSII activities of cyanobacterial preparations as well as the direct spectrophotometric measurement of TMPD photooxidation by PSI. The rates observed for PSI in this manner are compared to the rates measured in the traditional way as 02 uptake with excess ascorbate present. The impetus for the study was our interest in the photoreactions of the cyanelle of Cyanophora paradoxa, which although an endosymbiotic organelle, has the photochemical capabilities of cyanobacteria. The lability of the cyanelle PSII is shown as well as the ability of PSI to use ascorbate itself as a donor to a significant extent. This is in contrast to other photosynthetic systems in which ascorbate is a poor donor to PSI (4). MATERIALS AND METHODSSpinach was purchased from a local market. The methods used for growth of C. paradoxa and for isolation of the cyanelle were those previously described (8). The original culture of Phormidium laminosum (OH1-P), a gift from Dr. Richard Castenholz, was grown as described by Jackson and Castenholz (5). Spinach chloroplasts were prepared as previously reported (6) and finally suspended in 0.4 M sorbital and 0.1 M Tris buffer (pH 7.0). Photosynthetically active vesicles were prepared from cyanelles and from P. laminosum cells by treatment in a French Press at 14,000 p.s.i. in the medium described by Dilworth and Gantt (12) which contained 0.5 M sucrose, 0.5 M K-phosphate and 0.3 M sodium citrate, all at pH 7.0. This is designated SPC buffer. Serum albumin was not added, as was previously done by Katoh and Gantt (7). Better activity was observed for PSII if the final vesicle preparation contained 0.2 mg Chl/ml or more.PSII was assayed by DPIP photoreduction in...

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“…Their thylakoids are concentrically arranged as in some Oscillatoria species. In contrast, the genome size of cyanelles is only In the past, the cyanelle has often been considered as a bridge organism or an organelle in the evolution of chloroplasts from unicellular cyanobacteria (Klein et al, 1981;Was mann et al, 1987). Recently it has been stated that Prochloron or Prochlorothrix are better candidates for this (Morden and Golden, 1989) and that cyanelles more likely represent a side-line, dead-end in evolution (Kies and Kremer, 1990).…”

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confidence: 99%

The Cyanelles (Organelles of a Low Evolutionary Scale) Possess a Phosphate‐Translocator and a Glucose‐Carrier in Cyanophora paradoxa

Schlichting

Bothe

1993

Botanica Acta

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Cyanelles from Cyanophora paradoxa can easily be isolated and assayed for their carrier composition by the silicone oil filtering technique. The present investigation demonstrates a Pi‐translocator transferring phosphate, dihydroxyacetone phosphate and 3‐phosphoglycerate in a counter exchange mode in cyanelles as in chloroplasts of higher plants. The uptake of Pi is inhibited by dihydroxyacetone phosphate, phosphoglycerate and glucose‐6‐P, only poorly by phosphoenolpyruvate and not by 2‐phosphoglycerate. The inhibitors pyridoxalphosphate and 4,4′diisothiocyanostilbene‐2,2K'disulfonic acid at low concentration also affect Pi‐uptake. Cyanelles probably transport photosynthate (reductant and ATP) by triosephosphates. This is the first demonstration of a phosphate translocator in an organism of a low evolutionary scale. Cyanelles also transport glucose which proceeds in two phases. In the lower concentration range (≤ 2.5 mM), glucose penetrates by facilitated diffusion, whereas transport follows first‐order kinetics at higher amounts (> 2.5 mM). In the low concentration range, glucose‐transport is affected by high concentrations of 3‐O‐methylglucose and fructose. The physiological role of the glucose‐transport carrier in Cyanophora is doubtful. It may function in transporting glucose into cyanelles if the carbon level inside them becomes limiting, e.g. in dark periods.

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Properties of the Photosynthetic System and DNA of Cyanophora paradoxa Cyanelles

Cited by 8 publications

References 14 publications

Plastid Genomes from Diverse Glaucophyte Genera Reveal a Largely Conserved Gene Content and Limited Architectural Diversity

Plastid Genomes from Diverse Glaucophyte Genera Reveal a Largely Conserved Gene Content and Limited Architectural Diversity

Direct Spectrophotometric Measurement of Photosystem I and Photosystem II Activities of Photosynthetic Membrane Preparations from Cyanophora paradoxa, Phormidium laminosum, and Spinach

The Cyanelles (Organelles of a Low Evolutionary Scale) Possess a Phosphate‐Translocator and a Glucose‐Carrier in Cyanophora paradoxa

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