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The societal importance of renewable carbon-based commodities and energy carriers has elicited a particular interest for high performance phototrophic microorganisms. Selection of optimal strains is often based on direct comparison under laboratory conditions of maximal growth rate or additional valued features such as lipid content. Instead of reporting growth rate in culture, estimation of photosynthetic efficiency (quantum yield of PSII) by pulse-amplitude modulated (PAM) fluorimetry is an often applied alternative method. Here we compared the quantum yield of PSII and the photonic yield on biomass for the green alga Chlorella sorokiniana 211-8K and the cyanobacterium Synechocystis sp. PCC 6803. Our data demonstrate that the PAM technique inherently underestimates the photosynthetic efficiency of cyanobacteria by rendering a high F0 and a low FM, specifically after the commonly practiced dark pre-incubation before a yield measurement. Yet when comparing the calculated biomass yield on light in continuous culture experiments, we obtained nearly equal values for both species. Using mutants of Synechocystis sp. PCC 6803, we analyzed the factors that compromise its PAM-based quantum yield measurements. We will discuss the role of dark respiratory activity, fluorescence emission from the phycobilisomes, and the Mehler-like reaction. Based on the above observations we recommend that PAM measurements in cyanobacteria are interpreted only qualitatively.

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.

SignificanceCyanobacterial blooms pose a major threat to the water quality of many eutrophic lakes and reservoirs. Cyanobacteria are thought to be very effective competitors when CO2 levels are depleted during dense blooms. Their response to elevated CO2 is less understood, however. We study competition among cyanobacteria, and find both laboratory and field evidence for natural selection of strains with different carbon uptake systems at different CO2 levels. Our results demonstrate that changes in inorganic carbon availability act as an important selective factor in cyanobacterial communities and suggest that future harmful cyanobacterial blooms will have a genotype composition that differs from contemporary blooms and will be tuned to the high-CO2 conditions. Rising atmospheric CO2 concentrations are likely to affect many ecosystems worldwide. However, to what extent elevated CO2 will induce evolutionary changes in photosynthetic organisms is still a major open question. Here, we show rapid microevolutionary adaptation of a harmful cyanobacterium to changes in inorganic carbon (Ci) availability. We studied the cyanobacterium Microcystis, a notorious genus that can develop toxic cyanobacterial blooms in many eutrophic lakes and reservoirs worldwide. Microcystis displays genetic variation in the Ci uptake systems BicA and SbtA, where BicA has a low affinity for bicarbonate but high flux rate, and SbtA has a high affinity but low flux rate. Our laboratory competition experiments show that bicA + sbtA genotypes were favored by natural selection at low CO2 levels, but were partially replaced by the bicA genotype at elevated CO2. Similarly, in a eutrophic lake, bicA + sbtA strains were dominant when Ci concentrations were depleted during a dense cyanobacterial bloom, but were replaced by strains with only the high-flux bicA gene when Ci concentrations increased later in the season. Hence, our results provide both laboratory and field evidence that increasing carbon concentrations induce rapid adaptive changes in the genotype composition of harmful cyanobacterial blooms.

Mixotrophy is increasingly recognized as an important and widespread nutritional strategy in various taxonomic groups ranging from protists to higher plants. We hypothesize that the availability of alternative carbon and energy sources during mixotrophy allows a switch to photoheterotrophic growth, where the photosynthetic apparatus mainly provides energy but not fixed carbon. Because such a change in the function of the photosynthetic machinery is probably reflected in its composition, we compared the photosynthetic machinery in Ochromonas danica during autotrophic and mixotrophic growth. Compared with autotrophic growth, the total pigmentation of O. danica was reduced during mixotrophic growth. Furthermore, the photosystem I (PSI):PSII ratio increased, and the cellular content of Rubisco decreased not only absolutely, but also relative to the content of PSII. The changing composition of the photosynthetic apparatus indicates a shift in its function from providing both carbon and energy during photoautotrophy to mainly providing energy during mixotrophy. This preference for photoheterotrophic growth has interesting implications for the contribution of mixotrophic species to carbon cycling in diverse ecosystems.

Hydrogen peroxide (H2O2) can be used as an emergency method to selectively suppress cyanobacterial blooms in lakes and drinking water reservoirs. However, it is largely unknown how environmental parameters alter the effectiveness of H2O2 treatments. In this study, the toxic cyanobacterial strain Microcystis aeruginosa PCC 7806 was treated with a range of H2O2 concentrations (0 to 10 mg/L), while being exposed to different light intensities and light colors. H2O2 treatments caused a stronger decline of the photosynthetic yield in high light than in low light or in the dark, and also a stronger decline in orange than in blue light. Our results are consistent with the hypothesis that H2O2 causes major damage at photosystem II (PSII) and interferes with PSII repair, which makes cells more sensitive to photoinhibition. Furthermore, H2O2 treatments caused a decrease in cell size and an increase in extracellular microcystin concentrations, indicative of leakage from disrupted cells. Our findings imply that even low H2O2 concentrations of 1–2 mg/L can be highly effective, if cyanobacteria are exposed to high light intensities. We therefore recommend performing lake treatments during sunny days, when a low H2O2 dosage is sufficient to suppress cyanobacteria, and may help to minimize impacts on non-target organisms.

A method is presented for rapid extraction of the total plastoquinone (PQ) pool from Synechocystis sp. strain PCC 6803 cells that preserves the in vivo plastoquinol (PQH₂) to -PQ ratio. Cells were rapidly transferred into ice-cold organic solvent for instantaneous extraction of the cellular PQ plus PQH₂ content. After high-performance liquid chromatography fractionation of the organic phase extract, the PQH₂ content was quantitatively determined via its fluorescence emission at 330 nm. The in-cell PQH₂-PQ ratio then followed from comparison of the PQH₂ signal in samples as collected and in an identical sample after complete reduction with sodium borohydride. Prior to PQH₂ extraction, cells from steady-state chemostat cultures were exposed to a wide range of physiological conditions, including high/low availability of inorganic carbon, and various actinic illumination conditions. Wellcharacterized electron-transfer inhibitors were used to generate a reduced or an oxidized PQ pool for reference. The in vivo redox state of the PQ pool was correlated with the results of pulse-amplitude modulation-based chlorophyll a fluorescence emission measurements, oxygen exchange rates, and 77 K fluorescence emission spectra. Our results show that the redox state of the PQ pool of Synechocystis sp. strain PCC 6803 is subject to strict homeostatic control (i.e. regulated between narrow limits), in contrast to the more dynamic chlorophyll a fluorescence signal.

The ubiquitous chlorophyll a (Chl a) pigment absorbs both blue and red light. Yet, in contrast to green algae and higher plants, most cyanobacteria have much lower photosynthetic rates in blue than in red light. A plausible but not yet well-supported hypothesis is that blue light results in limited energy transfer to photosystem II (PSII), because cyanobacteria invest most Chl a in photosystem I (PSI), whereas their phycobilisomes (PBS) are mostly associated with PSII but do not absorb blue photons. In this paper, we compare the photosynthetic performance in blue and orange-red light of wildtype Synechocystis sp. PCC 6803 and a PBS-deficient mutant. Our results show that the wildtype had much lower biomass, Chl a content, PSI:PSII ratio and O2 production rate per PSII in blue light than in orange-red light, whereas the PBS-deficient mutant had a low biomass, Chl a content, PSI:PSII ratio, and O2 production rate per PSII in both light colors. More specifically, the wildtype displayed a similar low photosynthetic efficiency in blue light as the PBS-deficient mutant in both light colors. Our results demonstrate that the absorption of light energy by PBS and subsequent transfer to PSII are crucial for efficient photosynthesis in cyanobacteria, which may explain both the low photosynthetic efficiency of PBS-containing cyanobacteria and the evolutionary success of chlorophyll-based light-harvesting antennae in environments dominated by blue light.

In addition to their haloalkaline conditions, soda lakes can also harbor a variety of other extreme parameters, to which their microbial communities need to adapt. However, for most of these supplementary stressors, it is not well known yet how haloalkaliphiles adapt and resist. The genus Thioalkalivibrio comprises sulfur-oxidizing bacteria thriving in soda lakes at high pH and salinity. Depending on the geographical location and the season, these lakes can strongly vary in temperature. To obtain a comprehensive understanding of the molecular and physiological adaptations to low temperature, we compared the responses of two Thioalkalivibrio strains to low (10°C) and high (30°C) temperatures. For this, the strains were grown under controlled conditions in chemostats and analyzed for their gene expression (RNA sequencing [RNA-Seq]), membrane lipid composition, and glycine betaine content. The strain Thioalkalivibrio versutus AL2 T originated from a soda lake in southeast Siberia that is exposed to strong seasonal temperature differences, including freezing winters, whereas Thioalkalivibrio nitratis ALJ2 was isolated from an East African Rift Valley soda lake with a constant warm temperature the year round. The strain AL2 T grew faster than ALJ2 at 10°C, likely due to its 3-fold-higher concentration of the osmolyte glycine betaine. Moreover, significant changes in the membrane lipid composition were observed for both strains, leading to an increase in their unsaturated fatty acid content via the Fab pathway to avoid membrane stiffness. Genes for the transcriptional and translational machinery, as well as for counteracting cold-induced hampering of nucleotides and proteins, were upregulated. Oxidative stress was reduced by induction of vitamin B 12 biosynthesis genes, and growth at 10°C provoked downregulation of genes involved in the second half of the sulfur oxidation pathway. Genes for intracellular signal transduction were differentially expressed, and interestingly, AL2 T upregulated flagellin expression, whereas ALJ2 downregulated it. IMPORTANCE In addition to their haloalkaline conditions, soda lakes can also harbor a variety of other extreme parameters, to which their microbial communities need to adapt. However, for most of these supplementary stressors, it is not well known yet how haloalkaliphiles adapt and resist. Here, we studied the strategy for adaptation to low temperature in the haloalkaliphilic genus Thioalkalivibrio by using two strains isolated from soda lakes with different temperature regimes. Even though the strains showed a strong difference in growth rate at 10°C, they exhibited similar molecular and physiological adaptation responses. We hypothesize that they take advantage of resistance mechanisms against other stressors commonly found in soda lakes, which are therefore maintained in the bacteria living in the absence of low-temperature pressure. A major difference, however, was detected for their glycine betaine content at 10°C, highlighting the power of this osmolyte to also act as a key compound in cryoprotection. Author Video: An author video summary of this article is available.

The color of many lakes and seas is changing, which is likely to affect the species composition of freshwater and marine phytoplankton communities. For example, cyanobacteria with phycobilisomes as light-harvesting antennae can effectively utilize green or orange-red light. However, recent studies show that they use blue light much less efficiently than phytoplankton species with chlorophyll-based light-harvesting complexes, even though both phytoplankton groups may absorb blue light to a similar extent. Can we advance ecological theory to predict how these differences in light-harvesting strategy affect competition between phytoplankton species? Here, we develop a new resource competition model in which the absorption and utilization efficiency of different colors of light are varied independently. The model was parameterized using monoculture experiments with a freshwater cyanobacterium and green alga, as representatives of phytoplankton with phycobilisome-based vs. chlorophyll-based light-harvesting antennae. The parameterized model was subsequently tested in a series of competition experiments. In agreement with the model predictions, the green alga won the competition in blue light whereas the cyanobacterium won in red light, irrespective of the initial relative abundances of the species. These results are in line with observed changes in phytoplankton community structure in response to lake brownification. Similarly, in marine waters, the model predicts dominance of Prochlorococcus with chlorophyll-based light-harvesting complexes in blue light but dominance of Synechococcus with phycobilisomes in green light, with a broad range of coexistence in between. These predictions agree well with the known biogeographical distributions of these two highly abundant marine taxa. Our results offer a novel trait-based approach to understand and predict competition between phytoplankton species with different photosynthetic pigments and light-harvesting strategies.

The approach of providing an oxygenic photosynthetic organism with a cyclic electron transfer system, i.e., a far-red light-driven proton pump, is widely proposed to maximize photosynthetic efficiency via expanding the absorption spectrum of photosynthetically active radiation. As a first step in this approach, rhodopsin was expressed in a PSI-deletion strain of sp. PCC6803. Functional expression of rhodopsin, in contrast to Proteorhodopsin, did not stimulate the rate of photoheterotrophic growth of this strain, analyzed with growth rate measurements and competition experiments. Nevertheless, analysis of oxygen uptake and-production rates of the rhodopsin-expressing strains, relative to the ΔPSI control strain, confirm that the proton-pumping rhodopsin provides the cells with additional capacity to generate proton motive force. Significantly, expression of the rhodopsin did modulate levels of pigment formation in the transgenic strain.