Photosynthesis‐driven methane production in oxic lake water as an important contributor to methane emission

Authors

Marco Günthel Isabell Klawonn Jason Woodhouse Mina Bižić Danny Ionescu Lars Ganzert Steffen Kümmel Ivonne Nijenhuis Luca Zoccarato Hans‐Peter Grossart Kam W. Tang

Recent discovery of methane (CH₄) production in oxic waters challenges the conventional understanding of strict anoxic requirement for biological CH₄ production. High‐resolution field measurements in Lake Stechlin, as well as incubation experiments, suggested that oxic‐water CH₄ production occurred throughout much of the water column and was associated with phytoplankton especially diatoms, cyanobacteria, green algae, and cryptophytes. In situ concentrations and δ¹³C values of CH₄ in oxic water were negatively correlated with soluble reactive phosphorus concentrations. Using ¹³C‐labeling techniques, we showed that bicarbonate was converted to CH₄, and the production exceeded oxidation at day, but was comparable at night. These experimental data, along with complementary field observations, indicate a clear link between photosynthesis and the CH₄ production‐consumption balance in phosphorus‐limited epilimnic waters. Comparison between surface CH₄ emission data and experimental CH₄ production rates suggested that the oxic CH₄ source significantly contributed to surface emission in Lake Stechlin. These findings call for re‐examination of the aquatic CH₄ cycle and climate predictions.

The diversity and distribution of D1 proteins in cyanobacteria

Authors

Kevin J. Sheridan, Elizabeth J. Duncan, Julian J. Eaton-Rye & Tina C. Summerfield

The psbA gene family in cyanobacteria encodes different forms of the D1 protein that is part of the Photosystem II reaction centre. We have identified a phylogenetically distinct D1 group that is intermediate between previously identified G3-D1 and G4-D1 proteins (Cardona et al. Mol Biol Evol 32:1310–1328, 2015). This new group contained two subgroups: D1^INT, which was frequently in the genomes of heterocystous cyanobacteria and D1^FR that was part of the far-red light photoacclimation gene cluster of cyanobacteria. In addition, we have identified subgroups within G3, the micro-aerobically expressed D1 protein. There are amino acid changes associated with each of the subgroups that might affect the function of Photosystem II. We show a phylogenetically broad range of cyanobacteria have these D1 types, as well as the genes encoding the G2 protein and chlorophyll f synthase. We suggest identification of additional D1 isoforms and the presence of multiple D1 isoforms in phylogenetically diverse cyanobacteria supports the role of these proteins in conferring a selective advantage under specific conditions.

 

Measuring photosynthesis of both oxygenic and anoxygenic photosynthetic organisms using pulse amplitude modulation (PAM) fluorometry in wastewater ponds

Authors

P. Chandaravithoon, R. J. Ritchie & J. W. Runcie

Oxygenic photosynthesis can be measured easily using O₂ or CO₂ gas exchange, oxygen electrodes, Winkler titration, ¹⁴CO₂-fixation and by PAM (pulse amplitude modulation) fluorometry. PAM estimates the photosynthetic electron transport rate (ETR) by measuring the variable fluorescence of chlorophyll (Chl) a (> 695 nm) induced by absorption of blue or red light. Anoxygenic photosynthetic bacteria (APB) do not use water as an electron source and are typically photoheterotrophic rather than photoautotrophic and so ¹⁴CO₂ fixation is a misleading estimate of photosynthetic electron transport in APB photosynthesis. In vivo bacteriochlorophyll a (BChl a) absorbs blue light similar to Chl a but its characteristic longer-wavelength absorption is in the infrared and fluorescence is at > 800 nm. Blue light-induced PAM fluorescence can be used to measure the ETR in purple non-sulphur anoxygenic photobacteria and purple sulphur photobacteria because their RC-2 type BChl a complexes fluoresce similarly to PSII but at longer wavelengths than Chl a. Conventional PAM fluorometers using blue light cannot readily distinguish between oxygenic and RC-2 type anoxygenic photosynthesis because they use a simple > 700 nm highpass filter in front of the detector diode. We modified one fluorometer to use a 695–750-nm bandpass filter to measure Chl a fluorescence from PS-II, representing oxygenic photosynthesis. Similarly, we modified another fluorometer to use a highpass filter (> 830 nm) to measure BChl a fluorescence, representing anoxygenic photosynthesis. However, the fluorescence bands of Chl a and BChl a were found to be too wide to unambiguously distinguish between oxygenic and anoxygenic photosynthesis purely by fluorometry. Treatment with the specific PS-II inhibitor DCMU (Diuron) did enable discrimination of the two types of photosynthesis in a mixture of oxygenic and anoxygenic organisms. Ecological niches made up of both oxygenic and anoxygenic organisms such as microbial mats and hypereutrophic environments such as sewage ponds, wastewater ponds and prawn farm ponds are much more common than often realized. Anoxygenic photosynthesis in such systems is significant yet largely unquantified.

 

Color Sensing and Signal Transmission Diversity of Cyanobacterial Phytochromes and Cyanobacteriochromes

Authors

Yvette Villafani , Hee Wook Yang , and Youn-Il Park

To perceive fluctuations in light quality, quantity, and timing, higher plants have evolved diverse photoreceptors including UVR8 (a UV-B photoreceptor), cryptochromes, phototropins, and phytochromes (Phys). In contrast to plants, prokaryotic oxygen-evolving photosynthetic organisms, cyanobacteria, rely mostly on bilin-based photoreceptors, namely, cyanobacterial phytochromes (Cphs) and cyanobacteriochromes (CBCRs), which exhibit structural and functional differences compared with plant Phys. CBCRs comprise varying numbers of light sensing domains with diverse color-tuning mechanisms and signal transmission pathways, allowing cyanobacteria to respond to UV-A, visible, and far-red lights. Recent genomic surveys of filamentous cyanobacteria revealed novel CBCRs with broader chromophore-binding specificity and photocycle protochromicity. Furthermore, a novel Cph lineage has been identified that absorbs blue-violet/yellow-orange light. In this minireview, we briefly discuss the diversity in color sensing and signal transmission mechanisms of Cphs and CBCRs, along with their potential utility in the field of optogenetics.

Structure of a cyanobacterial photosystem I surrounded by octadecameric IsiA antenna proteins

Authors

Fusamichi Akita, Ryo Nagao, Koji Kato, Yoshiki Nakajima, Makio Yokono, Yoshifumi Ueno, Takehiro Suzuki, Naoshi Dohmae, Jian-Ren Shen, Seiji Akimoto & Naoyuki Miyazaki

Iron-stress induced protein A (IsiA) is a chlorophyll-binding membrane-spanning protein in photosynthetic prokaryote cyanobacteria, and is associated with photosystem I (PSI) trimer cores, but its structural and functional significance in light harvesting remains unclear. Here we report a 2.7-Å resolution cryo-electron microscopic structure of a supercomplex between PSI core trimer and IsiA from a thermophilic cyanobacterium Thermosynechococcus vulcanus. The structure showed that 18 IsiA subunits form a closed ring surrounding a PSI trimer core. Detailed arrangement of pigments within the supercomplex, as well as molecular interactions between PSI and IsiA and among IsiAs, were resolved. Time-resolved fluorescence spectra of the PSI–IsiA supercomplex showed clear excitation-energy transfer from IsiA to PSI, strongly indicating that IsiA functions as an energy donor, but not an energy quencher, in the supercomplex. These structural and spectroscopic findings provide important insights into the excitation-energy-transfer and subunit assembly mechanisms in the PSI–IsiA supercomplex.

Warming and CO2 effects under oligotrophication on temperate phytoplankton communities

Authors

Marco J. Cabrerizo, M. Inmaculada Álvarez-Manzaneda, Elizabeth León-Palmero, Gerardo Guerrero-Jiménez, Lisette N. de Senerpont Domis, Sven Teurlincx, Juan M. González-Olalla

Eutrophication, global warming, and rising carbon dioxide (CO₂) levels are the three most prevalent pressures impacting the biosphere. Despite their individual effects are well-known, it remains untested how oligotrophication (i.e. nutrients reduction) can alter the planktonic community responses to warming and elevated CO₂ levels. Here, we performed an indoor mesocosm experiment to investigate the warming × CO₂ interaction under a nutrient reduction scenario (40%) mediated by an in-lake management strategy (i.e. addition of a commercial solid-phase phosphorus sorbent -Phoslock®) on a natural freshwater plankton community. Biomass production increased under warming × CO₂ relative to present-day conditions; however, a Phoslock®-mediated oligotrophication reduced such values by 30–70%. Conversely, the warming × CO₂ × oligotrophication interaction stimulated the photosynthesis by 20% compared to ambient nutrient conditions, and matched with higher resource use efficiency (RUE) and nutrient demand. Surprisingly, at a group level, we found that the multi-stressors scenario increased the photosynthesis in eukaryotes by 25%, but greatly impaired in cyanobacteria (ca. −25%). This higher cyanobacterial sensitivity was coupled with a reduced light harvesting efficiency and compensation point. Since Phoslock®-induced oligotrophication unmasked a strong negative warming × CO₂ effect on cyanobacteria, it becomes crucial to understand how the interplay between climate change and nutrient abatement actions may alter the, ecosystems functioning. With an integrative understanding of these processes, policy makers will design more appropriate management strategies to improve the ecological status of aquatic ecosystems without compromising their ecological attributes and functioning.

A new strategy for a combined isolation of EPS and pigments from cyanobacteria

Authors

Strieth Dorina, Stiefelmaier Judith, Wrabl Björn, Schwing Julia, Schmeckebier Andrea, Di Nonno Sarah, Kai Muffler & Ulber Roland

Cyanobacteria obtain their energy through photosynthesis and live embedded in a matrix of extracellular polymeric substances (EPS) containing valuable products, e.g., polysaccharides, lipids, proteins, and antimicrobials. Besides chlorophyll a and carotenoids, they have light-absorbing compounds in the form of light-harvesting complexes, the so-called phycobilisomes, consisting of different phycobiliproteins. Together they close the “green gap” whereby cyanobacteria can use light more effective than higher plants. Cultivation of cyanobacteria on a lab-scale results in small amounts of biomass for their characterization or a comprehensive screening. EPS are, for example, produced as a protection against suboptimal culture conditions. Carotenoids are essential light-harvesting pigments for photosynthesis, play a key role in photoprotective reactions, and are produced for cell wall stabilization. Essentially, the pigment composition of cyanobacteria depends on the available light spectrum, nitrogen content, and temperature. Especially the production of EPS and pigments are indicators for the cell-condition. Therefore, different EPS extraction methods were tested including the determination of inhibitory effects of extracts against Escherichia coli. Based on the best EPS extraction method, a new strategy for downstream processing (DSP) was developed to determine EPS, the pigments chlorophyll a and carotenoids, and phycobiliproteins from only one sample. As cyanobacterial model organisms Trichocoleus sociatus and Nostoc flagelliforme were used, and DSP strategy was successfully transferred to four additional cyanobacteria. The final DSP includes the following steps: (i) EPS extraction, (ii) lyophilization of biomass, (iii) extraction of phycobiliproteins, and a final (iv) chlorophyll a and carotenoid extraction. The new strategy allows a comprehensive characterization of cyanobacterial cells.

Variation in phytoplankton pigment composition in relation to mixing conditions in temperate South-Central Chilean lake

Authors

Evelien Van de Vyver, Jeroen Van Wichelen, Pieter Vanormelingen, Wim Vannieuwenhuyze, Ilse Daveloose, Rixtde Jong, Reinhoudde Blok, Roberto Urrutia, Bjorn Tytgat, Elie Verleyen, Wim Vyverman

Thermal lake properties are sensitive to changes in windiness and precipitation, and affect the physical and chemical properties of the water column, which in turn control phytoplankton dynamics and primary production. We assessed the use of phytoplankton pigment profiling as a potential indicator of stratification conditions in temperate lakes in South-Central Chile. Spring and early summer phytoplankton pigment profiles and the physical and chemical limnology were analyzed in 43 lakes ranging in size, depth, altitude and catchment characteristics. Eleven lakes were sampled during both seasons. Variation in pigment composition between lakes was primarily related to stratification conditions and mixed layer light availability at the time of sampling. The dinoflagellate marker pigment peridinin was more abundant in more deeply mixed lakes with a lower mean irradiance, while chlorophyte pigments (chlorophyll b, lutein) tended to be higher in shallow (high-light) epilimnia. Diatom and chrysophyte pigments (fucoxanthin) dominated under less thermally stable and more variable light conditions. Cyanobacteria pigments (zeaxanthin), probably derived from picocyanobacteria, were relatively more abundant in very transparent, low productive lakes. Lakes in close vicinity of active volcanoes were enriched in silica and PO₄-P concentrations and characterised by elevated chlorophyte marker pigments. Within strongly stratified lakes, in which the euphotic zone extended in the hypolimnion, cryptophyte pigments (alloxanthin) characterized the deep chlorophyll maxima while the epilimnion was consistently enriched with the photoprotective xanthophyll-cycle pigment violaxanthin. We conclude that major algal groups, represented by pigment biomarkers, are largely driven by changes in lake water column stratification and related mixed layer light availability as well as nutrient concentrations in temperate Chilean freshwater lakes.

Stoichiometry and daily rhythms: experimental evidence shows nutrient limitation decouples N uptake from photosynthesis

Authors

Catherine A. Chamberlin, Emily S. Bernhardt, Emma J. Rosi, James B. Heffernan

Diel variability in nutrient concentrations is common but not universal in aquatic ecosystems. Theoretical models of photoautotrophic systems attribute the absence of diel uptake variation to nutrient scarcity, such that diel variability in nutrient uptake disappears as nutrients becomes limiting. We tested this prediction in a mesocosm experiment, by exposing benthic algal communities to a range of nitrogen (N) and phosphorus concentrations and recording the rates of uptake during both day and night. We found that higher concentrations of N produced diel variability in uptake, and that the difference between the day and night total mass uptakes approximately equaled N demand for observed primary production as seen in other studies. At lower concentrations of N, uptake rates during the day and night were indistinguishable. These results are the first empirical evidence to imply that diel nitrate patterns in streams and rivers indicate a release from N limitation and offer a new way to assess nutrient limitation.

Nitrogen transformations differentially affect nutrient‐limited primary production in lakes of varying trophic state

Authors

J. Thad Scott, Mark J. McCarthy, Hans W. Paerl

The concept of lakes “evolving” phosphorus (P) limitation has persisted in limnology despite limited direct evidence. Here, we developed a simple model to broadly characterize nitrogen (N) surpluses and deficits, relative to P, in lakes and compared the magnitude of this imbalance to estimates of N gains and losses through biological N transformations. The model suggested that approximately half of oligotrophic lakes in the U.S.A. had a stoichiometric N deficit, but 72–89% of eutrophic and hypereutrophic lakes, respectively, had a similar N deficit. Although reactive N appeared to accumulate in the most oligotrophic lakes, net denitrification perpetuated the N deficit in more productive lakes. Productive lakes exported reactive N via biological N transformations regardless of their N deficit. The lack of N accumulation through N fixation underscores the need for a modern eutrophication management approach focused on reducing total external nutrient loads, including both N and P.