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# Photosynthesis Research - Current Research Articles

## Current research articles: Photosynthesis

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... is an international journal open to papers of merit dealing with both basic and applied aspects of photosynthesis.

# Current articles of the journal:

## Amphiphilic, hydrophilic, or hydrophobic synthetic bacteriochlorins in biohybrid light-harvesting architectures: consideration of molecular designs

### Abstract

Biohybrid light-harvesting architectures can be constructed that employ native-like bacterial photosynthetic antenna peptides as a scaffold to which synthetic chromophores are attached to augment overall spectral coverage. Synthetic bacteriochlorins are attractive to enhance capture of solar radiation in the photon-rich near-infrared spectral region. The effect of the polarity of the bacteriochlorin substituents on the antenna self-assembly process was explored by the preparation of a bacteriochlorin–peptide conjugate using a synthetic amphiphilic bacteriochlorin (B1) to complement prior studies using hydrophilic (B2, four carboxylic acids) or hydrophobic (B3) bacteriochlorins. The amphiphilic bioconjugatable bacteriochlorin B1 with a polar ammonium-terminated tail was synthesized by sequential Pd-mediated reactions of a 3,13-dibromo-5-methoxybacteriochlorin. Each bacteriochlorin bears a maleimido-terminated tether for attachment to a cysteine-containing analog of the Rhodobacter sphaeroides antenna ?-peptide to give conjugates ?-B1, ?-B2, and ?-B3. Given the hydrophobic nature of the ?-peptide, the polarity of B1 and B2 facilitated purification of the respective conjugate compared to the hydrophobic B3. Bacteriochlorophyll a (BChl a) associates with each conjugate in aqueous micellar media to form a dyad containing two ?-peptides, two covalently attached synthetic bacteriochlorins, and a datively bonded BChl-a pair, albeit to a limited extent for ?-B2. The reversible assembly/disassembly of dyad (?-B2/BChl)2 was examined in aqueous detergent (octyl glucoside) solution by temperature variation (15–35 °C). The energy-transfer efficiency from the synthetic bacteriochlorin to the BChl-a dimer was found to be 0.85 for (?-B1/BChl)2, 0.40 for (?-B2/BChl)2, and 0.85 for (?-B3/BChl)2. Thus, in terms of handling, assembly and energy-transfer efficiency taken together, the amphiphilic design examined herein is more attractive than the prior hydrophilic or hydrophobic designs.

Posted on 1 November 2014 | 1:00 am

### Abstract

The aim of this educational review is to provide practical information on the hardware, methodology, and the hands on application of chlorophyll (Chl) a fluorescence technology. We present the paper in a question and answer format like frequently asked questions. Although nearly all information on the application of Chl a fluorescence can be found in the literature, it is not always easily accessible. This paper is primarily aimed at scientists who have some experience with the application of Chl a fluorescence but are still in the process of discovering what it all means and how it can be used. Topics discussed are (among other things) the kind of information that can be obtained using different fluorescence techniques, the interpretation of Chl a fluorescence signals, specific applications of these techniques, and practical advice on different subjects, such as on the length of dark adaptation before measurement of the Chl a fluorescence transient. The paper also provides the physiological background for some of the applied procedures. It also serves as a source of reference for experienced scientists.

Posted on 1 November 2014 | 1:00 am

## Alexander V. Ruban: The photosynthetic membrane: Molecular mechanisms and biophysics of light harvesting

Posted on 1 November 2014 | 1:00 am

## Unusual features of the high light acclimation of Chromera velia

### Abstract

In the present study, the high light (HL) acclimation of Chromera velia (Chromerida) was studied. HL-grown cells exhibited an increased cell volume and dry weight compared to cells grown at medium light (ML). The chlorophyll (Chl) a-specific absorption spectra ( $$a_{\text{phy}}^{*}$$ ) of the HL cells showed an increased absorption efficiency over a wavelength range from 400 to 750 nm, possibly due to differences in the packaging of Chl a molecules. In HL cells, the size of the violaxanthin (V) cycle pigment pool was strongly increased. Despite a higher concentration of de-epoxidized V cycle pigments, non-photochemical quenching (NPQ) of the HL cells was slightly reduced compared to ML cells. The analysis of NPQ recovery during low light (LL) after a short illumination with excess light showed a fast NPQ relaxation and zeaxanthin epoxidation. Purification of the pigment–protein complexes demonstrated that the HL-synthesized V was associated with the chromera light-harvesting complex (CLH). However, the difference absorption spectrum of HL minus ML CLH, together with the 77 K fluorescence excitation spectra, suggested that the additional V was not protein bound but localized in a lipid phase associated with the CLH. The polypeptide analysis of the pigment–protein complexes showed that one out of three known LHCr proteins was associated in higher concentration with photosystem I in the HL cells, whereas in ML cells, it was enriched in the CLH fraction. In conclusion, the acclimation of C. velia to HL illumination shows features that are comparable to those of diatoms, while other characteristics more closely resemble those of higher plants and green algae.

Posted on 1 November 2014 | 1:00 am

## Effect of surfactants on apparent oxygen consumption of photosystem I isolated from Arthrospira platensis

### Abstract

Surfactants play a significant role in solubilization of photosystem I (PSI) in vitro. Triton X-100 (TX), n-Dodecyl-?-d-maltoside (DDM), and sodium dodecyl sulfate (SDS) were employed to solubilize PSI particles in MES buffer to compare the effect of surfactant and its dosage on the apparent oxygen consumption rate of PSI. Through a combined assessment of sucrose density gradient centrifugation, Native PAGE and 77 K fluorescence with the apparent oxygen consumption, the nature of the enhancement of the apparent oxygen consumption activity of PSI by surfactants has been analyzed. Aggregated PSI particles can be dispersed by surfactant molecules into micelles, and the apparent oxygen consumption rate is higher for surfactant-solubilized PSI than for integral PSI particles. For DDM, PSI particles are solubilized mostly as the integral trimeric form. For TX, PSI particles are solubilized as incomplete trimeric and some monomeric forms. For the much harsher surfactant, SDS, PSI particles are completely solubilized as monomeric and its subunit forms. The enhancement of the oxygen consumption rate cannot be explained only by the effects of surfactant on the equilibrium between monomeric and trimeric forms of solubililized PSI. Care must be taken when the electron transfer activity of PSI is evaluated by methods based on oxygen consumption because the apparent oxygen consumption rate is influenced by uncoupled chlorophyll (Chl) from PSI, i.e., the larger the amount of uncoupled Chl, the higher the rate of apparent oxygen consumption. 77 K fluorescence spectra can be used to ensure that there is no uncoupled Chl present in the system. In order to eliminate the effect of trace uncoupled Chl, an efficient physical quencher of 1O2, such as 1 mM NaN3, may be added into the mixture.

Posted on 1 November 2014 | 1:00 am

## Phylogenetic analysis and molecular signatures defining a monophyletic clade of heterocystous cyanobacteria and identifying its closest relatives

### Abstract

Posted on 1 November 2014 | 1:00 am

## Interaction of ascorbate with photosystem I

### Abstract

Ascorbate is one of the key participants of the antioxidant defense in plants. In this work, we have investigated the interaction of ascorbate with the chloroplast electron transport chain and isolated photosystem I (PSI), using the EPR method for monitoring the oxidized centers $${\text{P}}_{700}^{ + }$$ and ascorbate free radicals. Inhibitor analysis of the light-induced redox transients of P700 in spinach thylakoids has demonstrated that ascorbate efficiently donates electrons to $${\text{P}}_{ 7 0 0}^{ + }$$ via plastocyanin. Inhibitors (DCMU and stigmatellin), which block electron transport between photosystem II and Pc, did not disturb the ascorbate capacity for electron donation to $${\text{P}}_{700}^{ + }$$ . Otherwise, inactivation of Pc with CN? ions inhibited electron flow from ascorbate to $${\text{P}}_{700}^{ + }$$ . This proves that the main route of electron flow from ascorbate to $${\text{P}}_{700}^{ + }$$ runs through Pc, bypassing the plastoquinone (PQ) pool and the cytochrome b 6 f complex. In contrast to Pc-mediated pathway, direct donation of electrons from ascorbate to $${\text{P}}_{700}^{ + }$$ is a rather slow process. Oxidized ascorbate species act as alternative oxidants for PSI, which intercept electrons directly from the terminal electron acceptors of PSI, thereby stimulating photooxidation of P700. We investigated the interaction of ascorbate with PSI complexes isolated from the wild type cells and the MenB deletion strain of cyanobacterium Synechocystis sp. PCC 6803. In the MenB mutant, PSI contains PQ in the quinone-binding A1-site, which can be substituted by high-potential electron carrier 2,3-dichloro-1,4-naphthoquinone (Cl2NQ). In PSI from the MenB mutant with Cl2NQ in the A1-site, the outflow of electrons from PSI is impeded due to the uphill electron transfer from A1 to the iron-sulfur cluster FX and further to the terminal clusters FA/FB, which manifests itself as a decrease in a steady-state level of $${\text{P}}_{700}^{ + }$$ . The addition of ascorbate promoted photooxidation of P700 due to stimulation of electron outflow from PSI to oxidized ascorbate species. Thus, accepting electrons from PSI and donating them to $${\text{P}}_{700}^{ + }$$ , ascorbate can mediate cyclic electron transport around PSI. The physiological significance of ascorbate-mediated electron transport is discussed.

Posted on 1 November 2014 | 1:00 am

## Proteomic approaches in research of cyanobacterial photosynthesis

### Abstract

Oxygenic photosynthesis in cyanobacteria, algae, and plants is carried out by a fabulous pigment-protein machinery that is amazingly complicated in structure and function. Many different approaches have been undertaken to characterize the most important aspects of photosynthesis, and proteomics has become the essential component in this research. Here we describe various methods which have been used in proteomic research of cyanobacteria, and demonstrate how proteomics is implemented into on-going studies of photosynthesis in cyanobacterial cells.

Posted on 31 October 2014 | 1:00 am

## Canopy light heterogeneity drives leaf anatomical, eco-physiological, and photosynthetic changes in olive trees grown in a high-density plantation

### Abstract

In the field, leaves may face very different light intensities within the tree canopy. Leaves usually respond with light-induced morphological and photosynthetic changes, in a phenomenon known as phenotypic plasticity. Canopy light distribution, leaf anatomy, gas exchange, chlorophyll fluorescence, and pigment composition were investigated in an olive (Olea europaea, cvs. Arbequina and Arbosana) orchard planted with a high-density system (1,250 trees ha?1). Sampling was made from three canopy zones: a lower canopy (<1 m), a central one (1–2 m), and an upper one (>2 m). Light interception decreased significantly in the lower canopy when compared to the central and top ones. Leaf angle increased and photosynthetic rates and non-photochemical quenching (NPQ) decreased significantly and progressively from the upper canopy to the central and the lower canopies. The largest leaf areas were found in the lower canopy, especially in the cultivar Arbequina. The palisade and spongy parenchyma were reduced in thickness in the lower canopy when compared to the upper one, in the former due to a decrease in the number of cell layers from three to two (clearly distinguishable in the light and fluorescence microscopy images). In both cultivars, the concentration of violaxanthin-cycle pigments and ?-carotene was higher in the upper than in the lower canopy. Furthermore, the de-epoxidized forms zeaxanthin and antheraxanthin increased significantly in those leaves from the upper canopy, in parallel to the NPQ increases. In conclusion, olive leaves react with morphological and photosynthetic changes to within-crown light gradients. These results strengthen the idea of olive trees as “modular organisms” that adjust the modules morphology and physiology in response to light intensity.

Posted on 26 October 2014 | 2:00 am

## Erratum to: Apparent PS II absorption cross-section and estimation of mean PAR in optically thin and dense suspensions of Chlorella

Posted on 16 October 2014 | 2:00 am

## Cadmium accumulation in chloroplasts and its impact on chloroplastic processes in barley and maize

### Abstract

Data on cadmium accumulation in chloroplasts of terrestrial plants are scarce and contradictory. We introduced CdSO4 in hydroponic media to the final concentrations 80 and 250 ?M and studied the accumulation of Cd in chloroplasts of Hordeum vulgare and Zea mays. Barley accumulated more Cd in the chloroplasts as compared to maize, whereas in the leaves cadmium accumulation was higher in maize. The cadmium content in the chloroplasts of two species varied from 49 to 171 ng Cd/mg chlorophyll, which corresponds to one Cd atom per 728–2,540 chlorophyll molecules. Therefore, Mg2+ can be substituted by Cd2+ in a negligible amount of antenna chlorophylls only. The percentage of chloroplastic cadmium can be estimated as 0.21–1.32 % of all the Cd in a leaf. Photochemistry (F v/F m, ?PSII, qP) was not influenced by Cd. Non-photochemical quenching of chlorophyll-excited state (NPQ) was greatly reduced in barley but not in maize. The decrease in NPQ was due to its fast relaxing component; the slow relaxing component rose slightly. In chloroplasts, Cd did not affect mRNA levels, but content of some photosynthetic proteins was reduced: slightly in the leaves of barley and heavily in the leaves of maize. In all analyzed C3-species, the effect of Cd on the content of photosynthetic proteins was mild or absent. This is most likely the first evidence of severe reduction of photosynthetic proteins in leaves of a Cd-treated C4-plant.

Posted on 15 October 2014 | 2:00 am

## A stable and efficient nuclear transformation system for the diatom Chaetoceros gracilis

### Abstract

Chaetoceros gracilis belongs to the centric diatoms, and has recently been used in basic research on photosynthesis. In addition, it has been commercially used in fisheries and is also attracting interest as a feedstock for biofuels production and biorefinery. In this study, we developed an efficient genetic transformation system for C. gracilis. The diatom cells were transformed via multi-pulse electroporation using plasmids containing various promoters to drive expression of the nourseothricin acetyltransferase gene (nat) as a selectable marker. The transformation efficiency reached ~400 positive transgenic clones per 108 recipient cells, which is the first example of successful transformation with electroporation in a centric diatom species. We further produced two expression vectors: the vector pCgLhcr5p contains the light-dependent promoter of a fucoxanthin chlorophyll a/c binding protein gene and the vector pCgNRp contains the inducible promoter of a nitrate reductase gene to drive the expression of introduced genes. In both vectors, an acetyl-CoA acetyltransferase promoter drives nat gene expression for antibiotic selection. Stable integration and expression of reporter genes, such as the firefly luciferase and green fluorescent protein Azami–Green genes, were observed in transformed C. gracilis cells. This efficient and stable transformation system for C. gracilis will enable both functional analysis of diatom-specific genes and strain improvement for further biotechnological applications.

Posted on 9 October 2014 | 2:00 am

## A loop unique to ferredoxin-dependent glutamate synthases is not absolutely essential for ferredoxin-dependent catalytic activity

### Abstract

It had been proposed that a loop, typically containing 26 or 27 amino acids, which is only present in monomeric, ferredoxin-dependent, “plant-type” glutamate synthases and is absent from the catalytic ?-subunits of both NADPH-dependent, heterodimeric glutamate synthases found in non-photosynthetic bacteria and NADH-dependent heterodimeric cyanobacterial glutamate synthases, plays a key role in productive binding of ferredoxin to the plant-type enzymes. Site-directed mutagenesis has been used to delete the entire 27 amino acid-long loop in the ferredoxin-dependent glutamate synthase from the cyanobacterium Synechocystis sp. PCC 6803. The specific activity of the resulting loopless variant of this glutamate synthase, when reduced ferredoxin serves as the electron donor, is actually higher than that of the wild-type enzyme, suggesting that this loop is not absolutely essential for efficient electron transfer from reduced ferredoxin to the enzyme. These results are consistent with the results of an in-silico study that suggests that the loop is unlikely to interact directly with ferredoxin in the energetically most favorable model of a 1:1 complex of ferredoxin with the wild-type enzyme.

Posted on 7 October 2014 | 2:00 am

## 13 C flux analysis of cyanobacterial metabolism

### Abstract

13C metabolic flux analysis (MFA) has made important contributions to our understanding of the physiology of model strains of E. coli and yeast, and it has been widely used to guide metabolic engineering efforts in these microorganisms. Recent advancements in 13C MFA methodology combined with publicly available software tools are creating new opportunities to extend this approach to examine less characterized microbes. In particular, growing interest in the use of cyanobacteria as industrial hosts for photosynthetic production of biofuels and biochemicals has led to a critical need to better understand how cyanobacterial metabolic fluxes are regulated in response to changes in growth conditions or introduction of heterologous pathways. In this contribution, we review several prior studies that have applied isotopic steady-state 13C MFA to examine heterotrophic or mixotrophic growth of cyanobacteria, as well as recent studies that have pioneered the use of isotopically nonstationary MFA (INST-MFA) to study autotrophic cultures. We also provide recommendations for the design and analysis of INST-MFA experiments in cyanobacteria, based on our previous experience and a series of simulation studies used to assess the selection of measurements and sample time points. We anticipate that this emerging knowledgebase of prior 13C MFA studies, optimized experimental protocols, and public software tools will catalyze increasing use of 13C MFA techniques by the cyanobacteria research community.

Posted on 4 October 2014 | 2:00 am

## Stories and photographs of William A. Arnold (1904–2001), a pioneer of photosynthesis and a wonderful friend

### Abstract

William A. Arnold discovered many phenomena in photosynthesis. In 1932, together with Robert Emerson, he provided the first experimental data that led to the concept of a large antenna and a few reaction centers (photosynthetic unit); in 1935, he obtained the minimum quantum requirement of 8–10 for the evolution of one O2 molecule; in 1951, together with Bernard L. Strehler, he discovered delayed fluorescence (also known as delayed light emission) in photosynthetic systems; and in 1956, together with Helen Sherwood, he discovered thermoluminescence in plants. He is also known for providing a solid-state picture of photosynthesis. Much has been written about him and his research, including many articles in a special issue of Photosynthesis Research (Govindjee et al. (eds.) 1996); and a biography of Arnold, by Govindjee and Srivastava (William Archibald Arnold (1904–2001), 2014), in the Biographical Memoirs of the US National Academy of Sciences, (Washington, DC). Our article here offers a glimpse into the everyday life, through stories and photographs, of this remarkable scientist.

Posted on 1 October 2014 | 2:00 am

## Supramolecular organization of photosynthetic membrane proteins in the chlorosome-containing bacterium Chloroflexus aurantiacus

### Abstract

The arrangement of core antenna complexes (B808-866-RC) in the cytoplasmic membrane of filamentous phototrophic bacterium Chloroflexus aurantiacus was studied by electron microscopy in cultures from different light conditions. A typical nearest-neighbor center-to-center distance of ~18 nm was found, implying less protein crowding compared to membranes of purple bacteria. A mean RC:chlorosome ratio of 11 was estimated for the occupancy of the membrane directly underneath each chlorosome, based on analysis of chlorosome dimensions and core complex distribution. Also presented are results of single-particle analysis of core complexes embedded in the native membrane.

Posted on 1 October 2014 | 2:00 am

## Fluorescence F 0 of photosystems II and I in developing C3 and C4 leaves, and implications on regulation of excitation balance

### Abstract

This work addresses the question of occurrence and function of photosystem II (PSII) in bundle sheath (BS) cells of leaves possessing NADP-malic enzyme-type C4 photosynthesis (Zea mays). Although no requirement for PSII activity in the BS has been established, several component proteins of PSII have been detected in BS cells of developing maize leaves exhibiting O2-insensitive photosynthesis. We used the basal fluorescence emissions of PSI (F 0I) and PSII (F 0II) as quantitative indicators of the respective relative photosystem densities. Chl fluorescence induction was measured simultaneously at 680 and 750 nm. In mature leaves, the F m(680)/F 0(680) ratio was 10.5 but less in immature leaves. We propose that the lower ratio was caused by the presence of a distinct non-variable component, F c, emitting at 680 and 750 nm. After F c was subtracted, the fluorescence of PSI (F 0I) was detected as a non-variable component at 750 nm and was undetectably low at 680 nm. Contents of Chls a and b were measured in addition to Chl fluorescence. The Chl b/(a + b) was relatively stable in developing sunflower leaves (0.25–0.26), but in maize it increased from 0.09 to 0.21 with leaf tissue age. In sunflower, the F 0I/(F 0I + F 0II) was 0.39 ± 0.01 independent of leaf age, but in maize, this parameter was 0.65 in young tissue of very low Chl content (20–50 mg m?2) falling to a stable level of 0.53 ± 0.01 at Chl contents >100 mg m?2. The values of F 0I/(F 0I + F 0II) showed that in sunflower, excitation was partitioned between PSII and PSI in a ratio of 2:1, but the same ratio was 1:1 in the C4 plant. The latter is consistent with a PSII:PSI ratio of 2:1 in maize mesophyll cells and PSI only in BS cells (2:1:1 distribution). We suggest, moreover, that redox mediation of Chl synthesis, rather than protein accumulation, regulates photosystem assembly to ensure optimum excitation balance between functional PSII and PSI. Indeed, the apparent necessity for two Chls (a and b) may reside in their targeted functions in influencing accumulation of PSI and PSII, respectively, as opposed to their spectral differences.

Posted on 1 October 2014 | 2:00 am

## Warwick Hillier: a tribute

### Abstract

Warwick Hillier (October 18, 1967–January 10, 2014) made seminal contributions to our understanding of photosynthetic water oxidation employing membrane inlet mass spectrometry and FTIR spectroscopy. This article offers a collection of historical perspectives on the scientific impact of Warwick Hillier’s work and tributes to the personal impact his life and ideas had on his collaborators and colleagues.

Posted on 1 October 2014 | 2:00 am

## Govindjee, an institution, at his 80th (really 81st) birthday in T?ebo? in October, 2013: a pictorial essay

### Abstract

Govindjee (one name only), who himself is an institution, has been recognized and honored by many in the past for he is a true ambassador of “Photosynthesis Research” to the World. He has been called “Mr. Photosynthesis”, and compared to the Great Wall of China. To us in T?ebo?, he has been a great research collaborator in our understanding of chlorophyll a fluorescence in algae and in cyanobacteria, and more than that a friend of the Czech “Photosynthesis” group, from the time of Ivan Šetlík (1928–2009) and of Zden?k Šesták (1932–2008). Govindjee’s 80th (really 81st) birthday was celebrated by the Institute of Microbiology, Laboratory of Photosynthesis, by toasting him with an appropriate drink of a suspension of green algae grown at the institute itself. After my presentation, on October 23, 2013, of Govindjee’s contributions to photosynthesis, and his intimate association with the photosynthetikers (in Jack Myers’s words) of the Czech Republic, Govindjee gave us his story of how he began research in photosynthesis in the late 1950s. This was followed by a talk on October 25 by him on “Photosynthesis: Stories of the Past.” Everyone enjoyed his animated talk—it was full of life and enjoyment. Here, I present a brief pictorial essay on Govindjee at his 80th (really 81st) birthday in T?ebo? during October 23–25, 2013.

Posted on 1 October 2014 | 2:00 am

## Crystal structure of CyanoQ from the thermophilic cyanobacterium Thermosynechococcus elongatus and detection in isolated photosystem II complexes

### Abstract

The PsbQ-like protein, termed CyanoQ, found in the cyanobacterium Synechocystis sp. PCC 6803 is thought to bind to the lumenal surface of photosystem II (PSII), helping to shield the Mn4CaO5 oxygen-evolving cluster. CyanoQ is, however, absent from the crystal structures of PSII isolated from thermophilic cyanobacteria raising the possibility that the association of CyanoQ with PSII might not be a conserved feature. Here, we show that CyanoQ (encoded by tll2057) is indeed expressed in the thermophilic cyanobacterium Thermosynechococcus elongatus and provide evidence in support of its assignment as a lipoprotein. Using an immunochemical approach, we show that CyanoQ co-purifies with PSII and is actually present in highly pure PSII samples used to generate PSII crystals. The absence of CyanoQ in the final crystal structure is possibly due to detachment of CyanoQ during crystallisation or its presence in sub-stoichiometric amounts. In contrast, the PsbP homologue, CyanoP, is severely depleted in isolated PSII complexes. We have also determined the crystal structure of CyanoQ from T. elongatus to a resolution of 1.6 Å. It lacks bound metal ions and contains a four-helix up-down bundle similar to the ones found in Synechocystis CyanoQ and spinach PsbQ. However, the N-terminal region and extensive lysine patch that are thought to be important for binding of PsbQ to PSII are not conserved in T. elongatus CyanoQ.

Posted on 1 October 2014 | 2:00 am