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CO 2 fertilization of terrestrial photosynthesis inferred from site to global scales

Significance The magnitude of the CO 2 fertilization effect on terrestrial photosynthesis is uncertain because it is not directly observed and is subject to confounding effects of climatic variability. We apply three well-established eco-evolutionary optimality theories of gas exchange and photosynthesis, constraining the main processes of CO 2 fertilization using measurable variables. Using this framework, we provide robust observationally inferred evidence that a strong CO 2 fertilization effect is detectable in globally distributed eddy covariance networks. Applying our method to upscale photosynthesis globally, we find that the magnitude of the CO 2 fertilization effect is comparable to its in situ counterpart but highlight the potential for substantial underestimation of this effect in tropical forests for many reflectance-based satellite photosynthesis products.

59 BASIC BIOLOGICAL SCIENCES↗

Conference Support, 32nd Western Photosynthesis Conference 2023

This DOE-BES award provided conference support for the 32nd Western Photosynthesis Conference (WPC2023), held January 5–8, 2023 at the Bodega Bay Marine Laboratory in Bodega Bay, California. The Western Photosynthesis Conference is one of three regional photosynthesis meetings held annually in the United States and serves as a primary venue for early-career scientists—graduate students, postdoctoral researchers, and undergraduates—to present research and build professional networks alongside established investigators in the field. Photosynthesis research is central to the DOE Office of Science's Basic Energy Sciences mission, underpinning fundamental understanding of solar energy conversion, biofuels, and the biological transformation of light into chemical energy. DOE-BES funds were used, as proposed, to support registration and housing costs for 20 early-career participants (9 postdoctoral researchers, 9 graduate students, and 2 undergraduates) and to help defray travel costs for two junior invited speakers based outside California, for a total DOE-BES expenditure of $10,060. The meeting was executed as planned, with no significant deviations from the approved program, budget, or schedule. WPC2023 drew 76 registrants across six scientific topic areas, featured 8 of 9 invited/keynote speakers, and provided extensive opportunities for early-career scientists to present talks and posters, compete for recognition awards, and network with senior researchers in the field.

conference↗

Carbon Dioxide Pressure and Catalyst Quantity Dependencies in Artificial Photosynthesis of Hydrocarbon Chains on Nanostructured Co/CoO Surfaces

In this study, we investigated the influence of pressure and the quantity of Co/CoO catalyst on an artificial photosynthesis process that converts CO 2 and H 2 O into hydrocarbons (C n H 2n+2 , where n ≤ 18). The adsorption of CO 2 and H 2 O on Co/CoO surfaces proved to be pivotal in this photo-catalytic reaction. Photoexcited carbon dioxide and water molecules ((CO 2 )* and (H 2 O)*) generated by illuminating the catalyst surface led to the formation of alkene hydrocarbon molecules with carbon numbers following an approximate Poisson distribution. The optimal pressure was found to be 0.40 MPa. Pressure less than 0.40 MPa resulted in low CO 2 adsorption, impeding excitation for photosynthesis. At greater pressure, oil/wax accumulation on Co/CoO surfaces hindered CO 2 adsorption, limiting further photosynthesis reactions. The average number of carbon atoms in the hydrocarbons and hydrocarbon yield were correlated. The amount of Co/CoO was also found to affect the hydrocarbon yield. Our study contributes to the understanding of Co/CoO-catalyzed photosynthesis and suggests that an open-flow system could potentially enhance the productivity of long-chain hydrocarbons.

59 BASIC BIOLOGICAL SCIENCES↗

Influence of sun zenith angle on canopy clumping and the resulting impacts on photosynthesis

Addressing the impact of vegetation architecture on shortwave radiation transfer in land surface models is important for accurate weather forecasting, carbon budget estimates, and climate predictions. This paper investigates to what extent it is possible to retrieve structural parameters of two different parameterization schemes from direct transmittance derived from digital hemispherical photography and 3D radiative transfer modeling for two study sites with different vegetation canopy architectures. Neglecting the representation of 3D canopy structure in radiative transfer schemes leads to significant errors in shortwave radiation partitioning (up to 3.5 times more direct transmittance in the 3D model). Structural parameters, referred to as whole canopy ‘clumping indices’, were obtained in order to evaluate the impact of angular variation in clumping on shortwave radiation transfer. Impacts on photosynthesis were evaluated at site level with the UKESM land surface model, JULES. A comparison between flux tower derived and modeled photosynthesis indicates that considering zenith angular variations of structural parameters in the radiative transfer scheme of the UKESM land surface model significantly improves photosynthesis prediction in light limited ecosystems (from RMSE = 2.91 μmol CO 2 .m -2 .s -1 to RMSE = 1.51 μmol CO 2 .m -2 .s -1 , 48% smaller), typically with enhanced photosynthesis from bottom layers.

54 ENVIRONMENTAL SCIENCES↗

Phenylene-linked tetrapyrrole arrays containing free base and diverse metal chelate forms – Versatile synthetic architectures for catalysis and artificial photosynthesis

Tetrapyrrole macrocycles are central to photosynthesis yet a single macrocycle does not carry out photosynthesis; rather, assemblies of tetrapyrrole macrocycles work in concert in antenna complexes, reaction centers, and electron-transport chains to harvest sunlight, funnel excited-state energy and separate charge for biological use. A longstanding theme in artificial photosynthesis has been to construct covalently linked “arrays” of metalated and free base tetrapyrrole macrocycles for fundamental studies of such processes, which entail excited-state and ground-state interactions. Among linkers in arrays chemistry, the 1,2-, 1,3-, or 1,4-disubstituted phenylene unit has proved very attractive owing to the resulting short distance, defined architecture, and appropriate extent of electronic coupling of adjacent macrocycles to give rapid electron and/or energy transfer while largely retaining desired spectral features. Eight distinct strategies to construct phenylene-linked tetrapyrrole arrays are identified in a review with comprehensive coverage since inception in the early 1970s through mid-year 2021. The arrays predominantly incorporate porphyrins with very few chlorins and bacteriochlorins, reflecting historic availability of synthetic methods for macrocycle formation. Of the eight strategies, only two appear applicable to (bacterio)chlorins. While studies in artificial photosynthesis have largely fueled this field, applications in catalysis have also been examined. Altogether >400 arrays are covered. The review delves into synthesis and molecular design, sketches photophysical properties, and suggests unrealized opportunities in arrays chemistry.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

Phenology of Photosynthesis in Winter‐Dormant Temperate and Boreal Forests: Long‐Term Observations From Flux Towers and Quantitative Evaluation of Phenology Models

Abstract We examined the seasonality of photosynthesis in 46 evergreen needleleaf (evergreen needleleaf forests (ENF)) and deciduous broadleaf (deciduous broadleaf forests (DBF)) forests across North America and Eurasia. We quantified the onset and end (Start GPP and End GPP ) of photosynthesis in spring and autumn based on the response of net ecosystem exchange of CO 2 to sunlight. To test the hypothesis that snowmelt is required for photosynthesis to begin, these were compared with end of snowmelt derived from soil temperature. ENF forests achieved 10% of summer photosynthetic capacity ∼3 weeks before end of snowmelt, while DBF forests achieved that capacity ∼4 weeks afterward. DBF forests increased photosynthetic capacity in spring faster (1.95% d −1 ) than ENF (1.10% d −1 ), and their active season length (End GPP –Start GPP ) was ∼50 days shorter. We hypothesized that warming has influenced timing of the photosynthesis season. We found minimal evidence for long‐term change in Start GPP , End GPP , or air temperature, but their interannual anomalies were significantly correlated. Warmer weather was associated with earlier Start GPP (1.3–2.5 days °C −1 ) or later End GPP (1.5–1.8 days °C −1 , depending on forest type and month). Finally, we tested whether existing phenological models could predict Start GPP and End GPP . For ENF forests, air temperature‐ and daylength‐based models provided best predictions for Start GPP , while a chilling‐degree‐day model was best for End GPP . The root mean square errors (RMSE) between predicted and observed Start GPP and End GPP were 11.7 and 11.3 days, respectively. For DBF forests, temperature‐ and daylength‐based models yielded the best results (RMSE 6.3 and 10.5 days).

Environmental Sciences & Ecology↗

Atmospheric Feedbacks Reverse the Sensitivity of Modeled Photosynthesis to Stomatal Function

Stomata mediate fluxes of carbon and water between terrestrial plants and the atmosphere. These fluxes are governed by stomatal function and can be modulated in many Earth system models by an empirical parameter within the calculation of stomatal conductance, the stomatal slope (𝑔 1⁢𝑀 ). Intuitively, 𝑔 1⁢𝑀 represents the marginal water cost of carbon, relating it to the emergent plant property of water use efficiency. Observations show that 𝑔 1⁢𝑀 can range widely across and within plant types in varying environments, and this distribution of 𝑔 1⁢𝑀 is not captured within Earth system models which represent each plant type with a single 𝑔 1⁢𝑀 value. Here we examine how 𝑔 1⁢𝑀 influences photosynthesis using coupled Earth system model simulations by perturbing 𝑔 1⁢𝑀 to observed 5⁢t⁢h and 95⁢t⁢h percentiles for each plant type. We find that high 𝑔 1⁢𝑀 reduces photosynthesis nearly everywhere, while low 𝑔 1⁢𝑀 has regionally dependent responses. Under fixed atmospheric conditions, low 𝑔 1⁢𝑀 increases photosynthesis in the Amazon and central North America but decreases photosynthesis in boreal Canada. These responses reverse when the atmosphere responds interactively due to spatially differing sensitivity to increases in temperature and vapor pressure deficit. Choice of 𝑔 1⁢𝑀 also influences photosynthetic response to changes in atmospheric carbon dioxide (CO 2 ), with lower and higher 𝑔1⁢𝑀 modifying total global response to elevated 2x preindustrial CO 2 by +6.4% and −9.6%, respectively. Our work demonstrates that atmospheric feedbacks are critical for determining the photosynthetic response to 𝑔 1⁢𝑀 assumptions and some regions are particularly sensitive to choice of 𝑔 1⁢𝑀 .

Liu, Amy X. [University of Washington, Seattle, WA↗

A constraint on historic growth in global photosynthesis due to rising CO 2

Theory predicts that rising CO 2 increases global photosynthesis, a process known as CO 2 fertilization, and that this is responsible for much of the current terrestrial carbon sink. The estimated magnitude of the historic CO 2 fertilization, however, differs by an order of magnitude between long-term proxies, remote sensing-based estimates and terrestrial biosphere models. Here we constrain the likely historic effect of CO 2 on global photosynthesis by combining terrestrial biosphere models, ecological optimality theory, remote sensing approaches and an emergent constraint based on global carbon budget estimates. Our analysis suggests that CO 2 fertilization increased global annual terrestrial photosynthesis by 13.5 ± 3.5% or 15.9 ± 2.9 PgC (mean ± s.d.) between 1981 and 2020. Our results help resolve conflicting estimates of the historic sensitivity of global terrestrial photosynthesis to CO 2 and highlight the large impact anthropogenic emissions have had on ecosystems worldwide.

54 ENVIRONMENTAL SCIENCES↗

Global evidence for the acclimation of ecosystem photosynthesis to light

Photosynthesis responds quickly to changes in light, increasing with incoming photosynthetic photon flux density (PPFD) until the leaves become light saturated. This instantaneous response to PPFD, which is widely studied and incorporated into models of photosynthesis, is overlaid on non-instantaneous photosynthetic changes resulting from the acclimation of plants to average PPFD over intermediate timescales of a week to months ($\overline{PPFD}$). Such photosynthetic light acclimation is not typically incorporated into models, due to the lack of observational constraints. In this work, we use eddy covariance observations from globally distributed and automated sensor networks, along with photosynthesis estimates from nine terrestrial biosphere models (TBMs), to quantify and assess photosynthetic acclimation to light in natural environments. We also use recent theoretical developments to incorporate light acclimation in a TBM. Our results show widespread light acclimation of ecosystem photosynthesis. On average, a 1 μmol m -2 s -1 increase in $\overline{PPFD}_{10}$ (ten-day average PPFD) leads to a 0.031 ± 0.013 μmol C m -2 s -1 increase in the maximum photosynthetic assimilation rate (A max ), with croplands having stronger acclimation rates than grasslands and forests. Our analysis shows that the TBMs examined either neglect or substantially underestimate light acclimation. By updating a TBM to include photosynthetic acclimation, successfully reproducing the $\overline{PPFD}_{10}$-A max relationship, we provide a robust method for the incorporation of photosynthetic light acclimation in future models.

59 BASIC BIOLOGICAL SCIENCES↗

Perspectives on improving photosynthesis to increase crop yield

Abstract Improving photosynthesis, the fundamental process by which plants convert light energy into chemical energy, is a key area of research with great potential for enhancing sustainable agricultural productivity and addressing global food security challenges. This perspective delves into the latest advancements and approaches aimed at optimizing photosynthetic efficiency. Our discussion encompasses the entire process, beginning with light harvesting and its regulation and progressing through the bottleneck of electron transfer. We then delve into the carbon reactions of photosynthesis, focusing on strategies targeting the enzymes of the Calvin–Benson–Bassham (CBB) cycle. Additionally, we explore methods to increase carbon dioxide (CO2) concentration near the Rubisco, the enzyme responsible for the first step of CBB cycle, drawing inspiration from various photosynthetic organisms, and conclude this section by examining ways to enhance CO2 delivery into leaves. Moving beyond individual processes, we discuss two approaches to identifying key targets for photosynthesis improvement: systems modeling and the study of natural variation. Finally, we revisit some of the strategies mentioned above to provide a holistic view of the improvements, analyzing their impact on nitrogen use efficiency and on canopy photosynthesis.

59 BASIC BIOLOGICAL SCIENCES↗

Alternative electron pathways of photosynthesis power green algal CO2 capture

Abstract Microalgae contribute to about half of global net photosynthesis, which converts sunlight into the chemical energy (ATP and NADPH) used to transform CO2 into biomass. Alternative electron pathways of photosynthesis have been proposed to generate additional ATP that is required to sustain CO2 fixation. However, the relative importance of each alternative pathway remains elusive. Here, we dissect and quantify the contribution of cyclic, pseudo-cyclic, and chloroplast-to-mitochondrion electron flows for their ability to sustain net photosynthesis in the microalga Chlamydomonas reinhardtii. We show that (i) each alternative pathway can provide sufficient additional energy to sustain high CO2 fixation rates, (ii) the alternative pathways exhibit cross-compensation, and (iii) the activity of at least one of the three alternative pathways is necessary to sustain photosynthesis. We further show that all pathways have very different efficiencies at energizing CO2 fixation, with the chloroplast–mitochondrion interaction being the most efficient. Overall, our data lay bioenergetic foundations for biotechnological strategies to improve CO2 capture and fixation.

Biochemistry & Molecular Biology↗

No evidence for a negative effect of growing season photosynthesis on leaf senescence timing

The length of the growing season has a large influence on the carbon, water, and energy fluxes of global terrestrial ecosystems. While there has been mounting evidence of an advanced start of the growing season mostly due to elevated spring air temperatures, the mechanisms that control the end of the growing season (EOS) in most ecosystems remain relatively less well understood. Recently, a strong lagged control of EOS by growing season photosynthesis has been proposed, suggesting that more productive growing seasons lead to an earlier EOS. However, this relationship has not been extensively tested with in-situ observations across a variety of ecosystems. In this work, we use observations from 40 eddy-covariance flux tower sites in temperate and boreal ecosystems in the northern hemisphere with more than 10 years of observations (594 site-years), ground observations of phenology, satellite observations from the Moderate Resolution Imaging Spectroradiometer (MODIS), and three leaf senescence models to test the extent of a relationship between growing season photosynthesis and end of season senescence. The results suggest that there is no significant negative relationship between growing season photosynthesis and observed leaf senescence, flux-inferred EOS estimates, or remotely sensed phenological metrics, in most ecosystems. On the contrary, while we found negative effects of summer air temperatures and autumn vapor pressure deficit on EOS, more productive growing seasons were typically related to a later, not earlier, EOS. Our results challenge recent reports of carry-over effects of photosynthesis on EOS timing, and suggest those results may not hold over a large range of ecosystems.

59 BASIC BIOLOGICAL SCIENCES↗

New-generation geostationary satellite reveals widespread midday depression in dryland photosynthesis during 2020 western U.S. heatwave

Emerging new-generation geostationary satellites have broadened the scope for studying the diurnal cycle of ecosystem functions. We exploit observations from the Geostationary Operational Environmental Satellite-R series to examine the effect of a severe U.S. heatwave in 2020 on the diurnal variations of ecosystem photosynthesis. We find divergent responses of photosynthesis to the heatwave across vegetation types and aridity gradients, with drylands exhibiting widespread midday and afternoon depression in photosynthesis. The diurnal centroid and peak time of dryland gross primary production (GPP) substantially shift toward earlier morning times, reflecting notable water and heat stress. Our geostationary satellite-based method outperforms traditional radiation-based upscaling methods from polar-orbiting satellite snapshots in estimating daily GPP and GPP loss during heatwaves. These findings underscore the potential of geostationary satellites for diurnal photosynthesis monitoring and highlight the necessity to consider the increased diurnal asymmetry in GPP under stress when evaluating carbon-climate interactions.

54 ENVIRONMENTAL SCIENCES↗

Mining Thermophile Photosynthesis Genes: A Synthetic Operon Expressing Chloroflexota Species Reaction Center Genes in Rhodobacter sphaeroides

Photosynthesis is the foundation of the vast majority of life systems, and is therefore the most important bioenergetic process on earth. The greatest diversity of photosynthetic systems is found in microorganisms. However, our understanding of the biophysical and biochemical processes that transduce light into chemical energy is derived from a relatively small subset of proteins from microbes that are amenable to cultivation, in contrast to the huge number of predicted proteins that catalyze the initial photochemical reactions deposited in databases, such as from metagenomics. We describe the use of a Rhodobacter sphaeroides laboratory strain for the expression of heterologous photosynthesis genes to demonstrate the feasibility of mining this resource, focusing on hot spring Chloroflexota gene sequences. Using a synthetic operon of genes, we produced a photochemically active complex of reaction center proteins in our biological system. We also present bioinformatic analyses of anoxygenic type II reaction center sequences from metagenomic samples collected from hot (42–90 °C) springs available through the JGI IMG database, to generate a resource of diverse sequences that are potentially adapted to photosynthesis at such temperatures. These data provide a view into the natural diversity of anoxygenic photosynthesis, through a lens focused on high-temperature environments. The approach we took to express such genes can be applied for potential biotechnology purposes as well as for studies of fundamental catalytic properties of these heretofore inaccessible protein complexes.

Chloroflexota↗

A double peak in the seasonality of California's photosynthesis as observed from space

Solar-induced chlorophyll fluorescence (SIF) has been shown to be a powerful proxy for photosynthesis and gross primary productivity (GPP). The recently launched TROPOspheric Monitoring Instrument (TROPOMI) features the required spectral resolution and signal-to-noise ratio to retrieve SIF from space. Here, we present a downscaling method to obtain 500 m spatial resolution SIF over California. We report daily values based on a 14 d window. TROPOMI SIF data show a strong correspondence with daily GPP estimates at AmeriFlux sites across multiple ecosystems in California. We find a linear relationship between SIF and GPP that is largely invariant across ecosystems with an intercept that is not significantly different from zero. Measurements of SIF from TROPOMI agree with MODerate Resolution Imaging Spectroradiometer (MODIS) vegetation indices – the normalized difference vegetation index (NDVI), enhanced vegetation index (EVI), and near-infrared reflectance of vegetation index (NIR$_v$) – at annual timescales but indicate different temporal dynamics at monthly and daily timescales. TROPOMI SIF data show a double peak in the seasonality of photosynthesis, a feature that is not present in the MODIS vegetation indices. The different seasonality in the vegetation indices may be due to a clear-sky bias in the vegetation indices, whereas previous work has shown SIF to have a low sensitivity to clouds and to detect the downregulation of photosynthesis even when plants appear green. We further decompose the spatiotemporal patterns in the SIF data based on land cover. The double peak in the seasonality of California's photosynthesis is due to two processes that are out of phase: grasses, chaparral, and oak savanna ecosystems show an April maximum, while evergreen forests peak in June. An empirical orthogonal function (EOF) analysis corroborates the phase offset and spatial patterns driving the double peak. The EOF analysis further indicates that two spatiotemporal patterns explain 84 % of the variability in the SIF data. Results shown here are promising for obtaining global GPP at sub-kilometer spatial scales and identifying the processes driving carbon uptake.

54 ENVIRONMENTAL SCIENCES↗

A differentiable, physics-informed ecosystem modeling and learning framework for large-scale inverse problems: demonstration with photosynthesis simulations

Photosynthesis plays an important role in carbon, nitrogen, and water cycles. Ecosystem models for photosynthesis are characterized by many parameters that are obtained from limited in situ measurements and applied to the same plant types. Previous site-by-site calibration approaches could not leverage big data and faced issues like overfitting or parameter non-uniqueness. Here we developed an end-to-end programmatically differentiable (meaning gradients of outputs to variables used in the model can be obtained efficiently and accurately) version of the photosynthesis process representation within the Functionally Assembled Terrestrial Ecosystem Simulator (FATES) model. As a genre of physics-informed machine learning (ML), differentiable models couple physics-based formulations to neural networks (NNs) that learn parameterizations (and potentially processes) from observations, here photosynthesis rates. We first demonstrated that the framework was able to correctly recover multiple assumed parameter values concurrently using synthetic training data. Then, using a real-world dataset consisting of many different plant functional types (PFTs), we learned parameters that performed substantially better and greatly reduced biases compared to literature values. Further, the framework allowed us to gain insights at a large scale. Our results showed that the carboxylation rate at 25 °C (V c,max25 ) was more impactful than a factor representing water limitation, although tuning both was helpful in addressing biases with the default values. This framework could potentially enable substantial improvement in our capability to learn parameters and reduce biases for ecosystem modeling at large scales.

54 ENVIRONMENTAL SCIENCES↗

Canopy reflectance, photosynthesis, and transpiration. II - The role of biophysics in the linearity of their interdependence

The ability of satellite sensor systems to estimate area-averaged canopy photosynthetic and transpirative properties is evaluated. The near linear relationship between the simple ratio (SR) and normalized difference (ND) and the surface biophysical properties of canopy photosynthetically active radiation (PAR) absorption, photosynthesis, and bulk stomatal resistance is studied. The models utilized to illustrate the processes of canopy reflectance, photosynthesis, and resistance are described. The dependence of SR, the absorbed fraction of PAR, and canopy photosynthesis and resistance on total leaf area index is analyzed. It is noted that the SR and ND vegetation indices and vegetation-dependent qualities are near-linearly related due to the proportion of leaf scattering coefficient in visible and near IR wavelength regions. The data reveal that satellite sensor systems are useful for the estimation of photosynthesis and transpirative properties.

Sellers, P. J.↗

Hydrogen peroxide and the evolution of oxygenic photosynthesis

Possible pathways for the evolution of oxygenic photosynthesis in the early reducing atmosphere of the earth are discussed. It is suggested that the abiotic production of atmospheric oxidants could have provided a mechanism by which locally oxidizing conditions were sustained within spatially confined habitats thus removing the available reductants and forcing photosynthetic organisms to utilize water (rather than ferrous or sulfide ions) as the electron donor. It is argued that atmospheric H2O2 played the key role in inducing oxygenic photosynthesis, because, as peroxide concentrations local environments increased, primitive organisms would not only be faced with a loss of a reductant, but would be also forced to develop a biochemical apparatus (such as catalase) that would protect them against the products of oxygenic photosynthesis. This scenario allows for the early evolution of oxygenic photosynthesis at the time when global conditions were still anaerobic.

Mckay, C. P.↗