Photosynthesis Research (v.138, #2)

In memory of Thomas Turpin Bannister (1930–2018) by Edward Laws; Alan Weidemann; George Hoch; Horatio Bannister; Robert S. Knox; Govindjee (129-138).
Tom Bannister (1930–2018) was an extraordinary person and a remarkably productive scientist. He began his career studying the basics of photochemistry, biophysics, and biology of photosynthetic pigments and later moved on to primary production of algae. His publications on modeling of primary production rates in aquatic systems are among the most widely cited in the field of phytoplankton ecology. His scientific enthusiasm was contagious, and his knowledge of photosynthesis and phytoplankton ecology enabled him to wisely mentor an impressive group of graduate students. He encouraged his students to strike out on their own but was always supportive and caring. Tom had a great love of life and nature, and he had a wonderful sense of humor. His students and those with whom he interacted remember him with great fondness. We have included here remembrances from some of us as well as from Rich Dempsey; Michael (Mike) Johnson; Stephen Lien; Janet Pelley; Bruce Selman; and Rudy Slovacek.
Keywords: Photosynthesis; Modeling; Light; Nutrients; Chlorophyll a fluorescence; Oxygenic photosynthesis; Phytoplankton ecology; Limnology

Pigment configuration in the light-harvesting protein of the xanthophyte alga Xanthonema debile by Simona Streckaite; Zdenko Gardian; Fei Li; Andrew A. Pascal; Radek Litvin; Bruno Robert; Manuel J. Llansola-Portoles (139-148).
The soil chromophyte alga Xanthonema (X.) debile contains only non-carbonyl carotenoids and Chl-a. X. debile has an antenna system denoted Xanthophyte light-harvesting complex (XLH) that contains the carotenoids diadinoxanthin, heteroxanthin, and vaucheriaxanthin. The XLH pigment stoichiometry was calculated by chromatographic techniques and the pigment-binding structure studied by resonance Raman spectroscopy. The pigment ratio obtained by HPLC was found to be close to 8:1:2:1 Chl-a:heteroxanthin:diadinoxanthin:vaucheriaxanthin. The resonance Raman spectra suggest the presence of 8–10 Chl-a, all of which are 5-coordinated to the central Mg, with 1–3 Chl-a possessing a macrocycle distorted from the relaxed conformation. The three populations of carotenoids are in the all-trans configuration. Vaucheriaxanthin absorbs around 500–530 nm, diadinoxanthin at 494 nm and heteroxanthin at 487 nm at 4.5 K. The effective conjugation length of heteroxanthin and diadinoxanthin has been determined as 9.4 in both cases; the environment polarizability of the heteroxanthin and diadinoxanthin binding pockets is 0.270 and 0.305, respectively.
Keywords: Light-harvesting complex; Algae; Resonance Raman; Chl-a ; Carotenoids; Diadinoxanthin; Heteroxanthin

Non-photochemical quenching (NPQ) is a fast acting photoprotective response to high light stress triggered by over excitation of photosystem II. The mechanism for NPQ in the globally important diatom algae has been principally attributed to a xanthophyll cycle, analogous to the well-described qE quenching of higher plants. This study compared the short-term NPQ responses in two pennate, benthic diatom species cultured under identical conditions but which originate from unique light climates. Variable chlorophyll fluorescence was used to monitor photochemical and non-photochemical excitation energy dissipation during high light transitions; whereas whole cell steady state 77 K absorption and emission were used to measure high light elicited changes in the excited state landscapes of the thylakoid. The marine shoreline species Nitzschia curvilineata was found to have an antenna system capable of entering a deeply quenched, yet reversible state in response to high light, with NPQ being highly sensitive to dithiothreitol (a known inhibitor of the xanthophyll cycle). Conversely, the salt flat species Navicula sp. 110-1 exhibited a less robust NPQ that remained largely locked-in after the light stress was removed; however, a lower amplitude, but now highly reversible NPQ persisted in cells treated with dithiothreitol. Furthermore, dithiothreitol inhibition of NPQ had no functional effect on the ability of Navicula cells to balance PSII excitation/de-excitation. These different approaches for non-photochemical excitation energy dissipation are discussed in the context of native light climate.
Keywords: Excitation pressure; Light harvesting; Non-photochemical quenching; Photoprotection

In framework of the continuum electrostatics theory, the reorganization energies of the electron transfers QA –QB (fast phase), Bph–QA, P+–QA , and P+–QB in the photosynthetic bacterial reaction center have been calculated. The calculations were based on the static dielectric permittivity spatial distribution derived from the data on the electrogenesis, with the corresponding characteristic times relatively close to the reaction times of QA –QB (fast phase) and Bph–QA but much shorter than those times of the latter two recombination reactions. The calculated reorganization energies were reasonably close to the experimental estimates for QA –QB (fast phase) and Bph–QA but substantially lower than those of P+–QA and P+–QB . A higher effective dielectric permittivity contributes to this effect, but the dominant contribution is most probably made by a non-dielectric relaxation, especially for the P+–QB recombination influenced by the proton transfer. This situation calls for reconsidering of the current electron transfer rate estimates.
Keywords: Photosynthesis; Quinone; Electron transfer; Reorganization energy; Dielectric inhomogeneity of protein

Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II by Veerle M. Luimstra; J. Merijn Schuurmans; Antonie M. Verschoor; Klaas J. Hellingwerf; Jef Huisman; Hans C. P. Matthijs (177-189).
Several studies have described that cyanobacteria use blue light less efficiently for photosynthesis than most eukaryotic phototrophs, but comprehensive studies of this phenomenon are lacking. Here, we study the effect of blue (450 nm), orange (625 nm), and red (660 nm) light on growth of the model cyanobacterium Synechocystis sp. PCC 6803, the green alga Chlorella sorokiniana and other cyanobacteria containing phycocyanin or phycoerythrin. Our results demonstrate that specific growth rates of the cyanobacteria were similar in orange and red light, but much lower in blue light. Conversely, specific growth rates of the green alga C. sorokiniana were similar in blue and red light, but lower in orange light. Oxygen production rates of Synechocystis sp. PCC 6803 were five-fold lower in blue than in orange and red light at low light intensities but approached the same saturation level in all three colors at high light intensities. Measurements of 77 K fluorescence emission demonstrated a lower ratio of photosystem I to photosystem II (PSI:PSII ratio) and relatively more phycobilisomes associated with PSII (state 1) in blue light than in orange and red light. These results support the hypothesis that blue light, which is not absorbed by phycobilisomes, creates an imbalance between the two photosystems of cyanobacteria with an energy excess at PSI and a deficiency at the PSII-side of the photosynthetic electron transfer chain. Our results help to explain why phycobilisome-containing cyanobacteria use blue light less efficiently than species with chlorophyll-based light-harvesting antennae such as Prochlorococcus, green algae and terrestrial plants.
Keywords: Blue light; Cyanobacteria; Photosynthesis; Photosystems; Phycobilisomes; Synechocystis PCC 6803

Simulation of chlorophyll fluorescence rise and decay kinetics, and P700-related absorbance changes by using a rule-based kinetic Monte-Carlo method by T. K. Antal; A. Maslakov; O. V. Yakovleva; T. E. Krendeleva; G. Yu. Riznichenko; A. B. Rubin (191-206).
A model of primary photosynthetic reactions in the thylakoid membrane was developed and its validity was tested by simulating three types of experimental kinetic curves: (1) the light-induced chlorophyll a fluorescence rise (OJIP transients) reflecting the stepwise transition of the photosynthetic electron transport chain from the oxidized to the fully reduced state; (2) the dark relaxation of the flash-induced fluorescence yield attributed to the QA oxidation kinetics in PSII; and (3) the light-induced absorbance changes near 820 or 705 nm assigned to the redox transitions of P700 in PSI. A model was implemented by using a rule-based kinetic Monte-Carlo method and verified by simulating experimental curves under different treatments including photosynthetic inhibitors, heat stress, anaerobic conditions, and very high light intensity.
Keywords: Monte-Carlo method; Photosynthesis model; Chlorophyll fluorescence; OJIP transients; Fluorescence decay; P700 redox transitions

In vivo regulation of thylakoid proton motive force in immature leaves by Wei Huang; Marjaana Suorsa; Shi-Bao Zhang (207-218).
In chloroplast, proton motive force (pmf) is critical for ATP synthesis and photoprotection. To prevent photoinhibition of photosynthetic apparatus, proton gradient (ΔpH) across the thylakoid membranes needs to be built up to minimize the production of reactive oxygen species (ROS) in thylakoid membranes. However, the regulation of thylakoid pmf in immature leaves is little known. In this study, we compared photosynthetic electron sinks, P700 redox state, non-photochemical quenching (NPQ), and electrochromic shift (ECS) signal in immature and mature leaves of a cultivar of Camellia. The immature leaves displayed lower linear electron flow and cyclic electron flow, but higher levels of NPQ and P700 oxidation ratio under high light. Meanwhile, we found that pmf and ΔpH were higher in the immature leaves. Furthermore, the immature leaves showed significantly lower thylakoid proton conductivity than mature leaves. These results strongly indicated that immature leaves can build up enough ΔpH by modulating proton efflux from the lumenal side to the stromal side of thylakoid membranes, which is essential to prevent photoinhibition via thermal energy dissipation and photosynthetic control of electron transfer. This study highlights that the activity of chloroplast ATP synthase is a key safety valve for photoprotection in immature leaves.
Keywords: Chloroplast ATP synthase; Electron transfer; Immature leaves; Lumenal acidification; P700 redox state; Photoprotection

Different CO2 acclimation strategies in juvenile and mature leaves of Ottelia alismoides by Wen Min Huang; Hui Shao; Si Ning Zhou; Qin Zhou; Wen Long Fu; Ting Zhang; Hong Sheng Jiang; Wei Li; Brigitte Gontero; Stephen C. Maberly (219-232).
The freshwater macrophyte, Ottelia alismoides, is a bicarbonate user performing C4 photosynthesis in the light, and crassulacean acid metabolism (CAM) when acclimated to low CO2. The regulation of the three mechanisms by CO2 concentration was studied in juvenile and mature leaves. For mature leaves, the ratios of phosphoenolpyruvate carboxylase (PEPC) to ribulose-bisphosphate carboxylase/oxygenase (Rubisco) are in the range of that of C4 plants regardless of CO2 concentration (1.5–2.5 at low CO2, 1.8–3.4 at high CO2). In contrast, results for juvenile leaves suggest that C4 is facultative and only present under low CO2. pH-drift experiments showed that both juvenile and mature leaves can use bicarbonate irrespective of CO2 concentration, but mature leaves have a significantly greater carbon-extracting ability than juvenile leaves at low CO2. At high CO2, neither juvenile nor mature leaves perform CAM as indicated by lack of diurnal acid fluctuation. However, CAM was present at low CO2, though the fluctuation of titratable acidity in juvenile leaves (15–17 µequiv g−1 FW) was slightly but significantly lower than in mature leaves (19–25 µequiv g−1 FW), implying that the capacity to perform CAM increases as leaves mature. The increased CAM activity is associated with elevated PEPC activity and large diel changes in starch content. These results show that in O. alismoides, carbon-dioxide concentrating mechanisms are more effective in mature compared to juvenile leaves, and C4 is facultative in juvenile leaves but constitutive in mature leaves.
Keywords: Bicarbonate use; C4 metabolism; Carbon dioxide-concentrating mechanism (CCM); Crassulacean acid metabolism (CAM); Freshwater macrophyte; Leaf maturity

Investigating the NAD-ME biochemical pathway within C4 grasses using transcript and amino acid variation in C4 photosynthetic genes by Alexander Watson-Lazowski; Alexie Papanicolaou; Robert Sharwood; Oula Ghannoum (233-248).
Expanding knowledge of the C4 photosynthetic pathway can provide key information to aid biological improvements to crop photosynthesis and yield. While the C4 NADP-ME pathway is well characterised, there is increasing agricultural and bioengineering interest in the comparably understudied NAD-ME and PEPCK pathways. Within this study, a systematic identification of key differences across species has allowed us to investigate the evolution of C4-recruited genes in one C3 and eleven C4 grasses (Poaceae) spanning two independent origins of C4 photosynthesis. We present evidence for C4-specific paralogs of NAD-malic enzyme 2, MPC1 and MPC2 (mitochondrial pyruvate carriers) via increased transcript abundance and associated rates of evolution, implicating them as genes recruited to perform C4 photosynthesis within NAD-ME and PEPCK subtypes. We then investigate the localisation of AspAT across subtypes, using novel and published evidence to place AspAT3 in both the cytosol and peroxisome. Finally, these findings are integrated with transcript abundance of previously identified C4 genes to provide an updated model for C4 grass NAD-ME and PEPCK photosynthesis. This updated model allows us to develop on the current understanding of NAD-ME and PEPCK photosynthesis in grasses, bolstering our efforts to understand the evolutionary ‘path to C4’ and improve C4 photosynthesis.
Keywords: C4 photosynthesis; Gene recruitment; Convergent evolution; Poaceae; NAD-ME; PEPCK

In this study, we examined interactive effects of elevated atmospheric CO2, concentrations, and increased tidal flooding on two mangroves species, Avicennia marina and Rhizophora stylosa. Leaf gas-exchange parameters (photosynthesis, transpiration rates, water-use efficiency, stomatal conductance, and dark respiration rates) were measured monthly on more than 1000 two-year-old seedlings grown in greenhouses for 1 year. In addition, stomatal density and light curve responses were determined at the end of the experiment. Under elevated CO2 concentrations (800 ppm), the net photosynthetic rates were enhanced by more than 37% for A. marina and 45% for R. stylosa. This effect was more pronounced during the warm season, suggesting that an increase in global temperatures would further enhance the photosynthetic response of the considered species. Transpiration rates decreased by more than 15 and 8% for A. marina and R. stylosa, respectively. Consequently, water-use efficiency increased by 76% and 98% for A. marina and R. stylosa, respectively, for both species, which will improve drought resistance. These responses to elevated CO2 were minimized (by 5%) with longer flooding duration. Consequently, future increases of atmospheric CO2 may have a strong and positive effect on juveniles of A. marina and R. stylosa during the next century, which may not be suppressed by the augmentation of tidal flooding duration induced by sea-level rise. It is possible that this effect will enhance seedling dynamic by increasing photosynthesis, and therefore will facilitate their settlements in new area, extending the role of mangrove ecosystems in carbon sequestration and climate change mitigation.
Keywords: Mangrove; CO2 enrichment; Photosynthetic activity; Stomatal density; Climate change; Sea-level rise