Biofuels for a sustainable future.

Rapid increases of energy consumption and human dependency on fossil fuels have led to the accumulation of greenhouse gases and consequently, climate change. As such, major efforts have been taken to develop, test, and adopt clean renewable fuel alternatives. Production of bioethanol and biodiesel from crops is well developed, while other feedstock resources and processes have also shown high potential to provide efficient and cost-effective alternatives, such as landfill and plastic waste conversion, algal photosynthesis, as well as electrochemical carbon fixation. In addition, the downstream microbial fermentation can be further engineered to not only increase the product yield but also expand the chemical space of biofuels through the rational design and fine-tuning of biosynthetic pathways toward the realization of "designer fuels" and diverse future applications.

A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism.

Approximately one-third of global CO2 fixation is performed by eukaryotic algae. Nearly all algae enhance their carbon assimilation by operating a CO2-concentrating mechanism (CCM) built around an organelle called the pyrenoid, whose protein composition is largely unknown. Here, we developed tools in the model alga Chlamydomonas reinhardtii to determine the localizations of 135 candidate CCM proteins and physical interactors of 38 of these proteins. Our data reveal the identity of 89 pyrenoid proteins, including Rubisco-interacting proteins, photosystem I assembly factor candidates, and inorganic carbon flux components. We identify three previously undescribed protein layers of the pyrenoid: a plate-like layer, a mesh layer, and a punctate layer. We find that the carbonic anhydrase CAH6 is in the flagella, not in the stroma that surrounds the pyrenoid as in current models. These results provide an overview of proteins operating in the eukaryotic algal CCM, a key process that drives global carbon fixation.

One-third of Southern Ocean productivity is supported by dust deposition.

Natural iron fertilization of the Southern Ocean by windblown dust has been suggested to enhance biological productivity and modulate the climate1-3. Yet, this process has never been quantified across the Southern Ocean and at annual timescales4,5. Here we combined 11 years of nitrate observations from autonomous biogeochemical ocean profiling floats with a Southern Hemisphere dust simulation to empirically derive the relationship between dust-iron deposition and annual net community production (ANCP) in the iron-limited Southern Ocean. Using this relationship, we determined the biological response to dust-iron in the pelagic perennially ice-free Southern Ocean at present and during the last glacial maximum (LGM). We estimate that dust-iron now supports 33% ± 15% of Southern Ocean ANCP. During the LGM, when dust deposition was 5-40-fold higher than today, the contribution of dust to Southern Ocean ANCP was much greater, estimated at 64% ± 13%. We provide quantitative evidence of basin-wide dust-iron fertilization of the Southern Ocean and the potential magnitude of its impact on glacial-interglacial timescales, supporting the idea of the important role of dust in the global carbon cycle and climate6-8.

Dearomatization drives complexity generation in freshwater organic matter.

Dissolved organic matter (DOM) is one of the most complex, dynamic and abundant sources of organic carbon, but its chemical reactivity remains uncertain1-3. Greater insights into DOM structural features could facilitate understanding its synthesis, turnover and processing in the global carbon cycle4,5. Here we use complementary multiplicity-edited 13C nuclear magnetic resonance (NMR) spectra to quantify key substructures assembling the carbon skeletons of DOM from four main Amazon rivers and two mid-size Swedish boreal lakes. We find that one type of reaction mechanism, oxidative dearomatization (ODA), widely used in organic synthetic chemistry to create natural product scaffolds6-10, is probably a key driver for generating structural diversity during processing of DOM that are rich in suitable polyphenolic precursor molecules. Our data suggest a high abundance of tetrahedral quaternary carbons bound to one oxygen and three carbon atoms (OCqC3 units). These units are rare in common biomolecules but could be readily produced by ODA of lignin-derived and tannin-derived polyphenols. Tautomerization of (poly)phenols by ODA creates non-planar cyclohexadienones, which are subject to immediate and parallel cycloadditions. This combination leads to a proliferation of structural diversity of DOM compounds from early stages of DOM processing, with an increase in oxygenated aliphatic structures. Overall, we propose that ODA is a key reaction mechanism for complexity acceleration in the processing of DOM molecules, creation of new oxygenated aliphatic molecules and that it could be prevalent in nature.

Environmental drivers of increased ecosystem respiration in a warming tundra.

Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5-7. This hampers the accuracy of global land carbon-climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9-2.0 °C] in air and 0.4 °C [CI 0.2-0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22-38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

The refinery of the future.

Fossil fuels-coal, oil and gas-supply most of the world's energy and also form the basis of many products essential for everyday life. Their use is the largest contributor to the carbon dioxide emissions that drive global climate change, prompting joint efforts to find renewable alternatives that might enable a carbon-neutral society by as early as 2050. There are clear paths for renewable electricity to replace fossil-fuel-based energy, but the transport fuels and chemicals produced in oil refineries will still be needed. We can attempt to close the carbon cycle associated with their use by electrifying refinery processes and by changing the raw materials that go into a refinery from fossils fuels to carbon dioxide for making hydrocarbon fuels and to agricultural and municipal waste for making chemicals and polymers. We argue that, with sufficient long-term commitment and support, the science and technology for such a completely fossil-free refinery, delivering the products required after 2050 (less fuels, more chemicals), could be developed. This future refinery will require substantially larger areas and greater mineral resources than is the case at present and critically depends on the capacity to generate large amounts of renewable energy for hydrogen production and carbon dioxide capture.

River ecosystem metabolism and carbon biogeochemistry in a changing world.

River networks represent the largest biogeochemical nexus between the continents, ocean and atmosphere. Our current understanding of the role of rivers in the global carbon cycle remains limited, which makes it difficult to predict how global change may alter the timing and spatial distribution of riverine carbon sequestration and greenhouse gas emissions. Here we review the state of river ecosystem metabolism research and synthesize the current best available estimates of river ecosystem metabolism. We quantify the organic and inorganic carbon flux from land to global rivers and show that their net ecosystem production and carbon dioxide emissions shift the organic to inorganic carbon balance en route from land to the coastal ocean. Furthermore, we discuss how global change may affect river ecosystem metabolism and related carbon fluxes and identify research directions that can help to develop better predictions of the effects of global change on riverine ecosystem processes. We argue that a global river observing system will play a key role in understanding river networks and their future evolution in the context of the global carbon budget.

Neogene burial of organic carbon in the global ocean.

Organic carbon buried in marine sediment serves as a net sink for atmospheric carbon dioxide and a source of oxygen1,2. The rate of organic carbon burial through geologic history is conventionally established by using the mass balance between inorganic and organic carbon, each with distinct carbon isotopic values (δ13C)3,4. This method is complicated by large uncertainties, however, and has not been tested with organic carbon accumulation data5,6. Here we report a 'bottom-up' approach for calculating the rate of organic carbon burial that is independent from mass balance calculations. We use data from 81 globally distributed sites to establish the history of organic carbon burial during the Neogene (roughly 23-3 Ma). Our results show larger spatiotemporal variability of organic carbon burial than previously estimated7-9. Globally, the burial rate is high towards the early Miocene and Pliocene and lowest during the mid-Miocene, with the latter period characterized by the lowest ratio of organic-to-carbonate burial rates. This is in contrast to earlier work that interpreted enriched carbonate 13C values of the mid-Miocene as massive organic carbon burial (that is, the Monterey Hypothesis)10,11. Suppressed organic carbon burial during the warm mid-Miocene is probably related to temperature-dependent bacterial degradation of organic matter12,13, suggesting that the organic carbon cycle acted as positive feedback of past global warming.

Photosynthesis re-wired on the pico-second timescale.

Photosystems II and I (PSII, PSI) are the reaction centre-containing complexes driving the light reactions of photosynthesis; PSII performs light-driven water oxidation and PSI further photo-energizes harvested electrons. The impressive efficiencies of the photosystems have motivated extensive biological, artificial and biohybrid approaches to 're-wire' photosynthesis for higher biomass-conversion efficiencies and new reaction pathways, such as H2 evolution or CO2 fixation1,2. Previous approaches focused on charge extraction at terminal electron acceptors of the photosystems3. Electron extraction at earlier steps, perhaps immediately from photoexcited reaction centres, would enable greater thermodynamic gains; however, this was believed impossible with reaction centres buried at least 4 nm within the photosystems4,5. Here, we demonstrate, using in vivo ultrafast transient absorption (TA) spectroscopy, extraction of electrons directly from photoexcited PSI and PSII at early points (several picoseconds post-photo-excitation) with live cyanobacterial cells or isolated photosystems, and exogenous electron mediators such as 2,6-dichloro-1,4-benzoquinone (DCBQ) and methyl viologen. We postulate that these mediators oxidize peripheral chlorophyll pigments participating in highly delocalized charge-transfer states after initial photo-excitation. Our results challenge previous models that the photoexcited reaction centres are insulated within the photosystem protein scaffold, opening new avenues to study and re-wire photosynthesis for biotechnologies and semi-artificial photosynthesis.

Authigenic mineral phases as a driver of the upper-ocean iron cycle.

Iron is important in regulating the ocean carbon cycle1. Although several dissolved and particulate species participate in oceanic iron cycling, current understanding emphasizes the importance of complexation by organic ligands in stabilizing oceanic dissolved iron concentrations2-6. However, it is difficult to reconcile this view of ligands as a primary control on dissolved iron cycling with the observed size partitioning of dissolved iron species, inefficient dissolved iron regeneration at depth or the potential importance of authigenic iron phases in particulate iron observational datasets7-12. Here we present a new dissolved iron, ligand and particulate iron seasonal dataset from the Bermuda Atlantic Time-series Study (BATS) region. We find that upper-ocean dissolved iron dynamics were decoupled from those of ligands, which necessitates a process by which dissolved iron escapes ligand stabilization to generate a reservoir of authigenic iron particles that settle to depth. When this 'colloidal shunt' mechanism was implemented in a global-scale biogeochemical model, it reproduced both seasonal iron-cycle dynamics observations and independent global datasets when previous models failed13-15. Overall, we argue that the turnover of authigenic particulate iron phases must be considered alongside biological activity and ligands in controlling ocean-dissolved iron distributions and the coupling between dissolved and particulate iron pools.

Increasingly negative tropical water-interannual CO2 growth rate coupling.

Terrestrial ecosystems have taken up about 32% of the total anthropogenic CO2 emissions in the past six decades1. Large uncertainties in terrestrial carbon-climate feedbacks, however, make it difficult to predict how the land carbon sink will respond to future climate change2. Interannual variations in the atmospheric CO2 growth rate (CGR) are dominated by land-atmosphere carbon fluxes in the tropics, providing an opportunity to explore land carbon-climate interactions3-6. It is thought that variations in CGR are largely controlled by temperature7-10 but there is also evidence for a tight coupling between water availability and CGR11. Here, we use a record of global atmospheric CO2, terrestrial water storage and precipitation data to investigate changes in the interannual relationship between tropical land climate conditions and CGR under a changing climate. We find that the interannual relationship between tropical water availability and CGR became increasingly negative during 1989-2018 compared to 1960-1989. This could be related to spatiotemporal changes in tropical water availability anomalies driven by shifts in El Niño/Southern Oscillation teleconnections, including declining spatial compensatory water effects9. We also demonstrate that most state-of-the-art coupled Earth System and Land Surface models do not reproduce the intensifying water-carbon coupling. Our results indicate that tropical water availability is increasingly controlling the interannual variability of the terrestrial carbon cycle and modulating tropical terrestrial carbon-climate feedbacks.

Aligning climate scenarios to emissions inventories shifts global benchmarks.

Taking stock of global progress towards achieving the Paris Agreement requires consistently measuring aggregate national actions and pledges against modelled mitigation pathways1. However, national greenhouse gas inventories (NGHGIs) and scientific assessments of anthropogenic emissions follow different accounting conventions for land-based carbon fluxes resulting in a large difference in the present emission estimates2,3, a gap that will evolve over time. Using state-of-the-art methodologies4 and a land carbon-cycle emulator5, we align the Intergovernmental Panel on Climate Change (IPCC)-assessed mitigation pathways with the NGHGIs to make a comparison. We find that the key global mitigation benchmarks become harder to achieve when calculated using the NGHGI conventions, requiring both earlier net-zero CO2 timing and lower cumulative emissions. Furthermore, weakening natural carbon removal processes such as carbon fertilization can mask anthropogenic land-based removal efforts, with the result that land-based carbon fluxes in NGHGIs may ultimately become sources of emissions by 2100. Our results are important for the Global Stocktake6, suggesting that nations will need to increase the collective ambition of their climate targets to remain consistent with the global temperature goals.

Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape.

An ultimate goal of evolutionary biology is the prediction and experimental verification of adaptive trajectories on macroevolutionary timescales. This aim has rarely been achieved for complex biological systems, as models usually lack clear correlates of organismal fitness. Here, we simulate the fitness landscape connecting two carbon fixation systems: C3 photosynthesis, used by most plant species, and the C4 system, which is more efficient at ambient CO2 levels and elevated temperatures and which repeatedly evolved from C3. Despite extensive sign epistasis, C4 photosynthesis is evolutionarily accessible through individually adaptive steps from any intermediate state. Simulations show that biochemical subtraits evolve in modules; the order and constitution of modules confirm and extend previous hypotheses based on species comparisons. Plant-species-designated C3-C4 intermediates lie on predicted evolutionary trajectories, indicating that they indeed represent transitory states. Contrary to expectations, we find no slowdown of adaptation and no diminishing fitness gains along evolutionary trajectories.

Biogenesis of a bacterial organelle: the carboxysome assembly pathway.

The carboxysome is a protein-based organelle for carbon fixation in cyanobacteria, keystone organisms in the global carbon cycle. It is composed of thousands of subunits including hexameric and pentameric proteins that form a shell to encapsulate the enzymes ribulose 1,5-bisphosphate carboxylase/oxygenase and carbonic anhydrase. Here, we describe the stages of carboxysome assembly and the requisite gene products necessary for progression through each. Our results demonstrate that, unlike membrane-bound organelles of eukaryotes, in carboxysomes the interior of the compartment forms first, at a distinct site within the cell. Subsequently, shell proteins encapsulate this procarboxysome, inducing budding and distribution of functional organelles within the cell. We propose that the principles of carboxysome assembly that we have uncovered extend to diverse bacterial microcompartments.

Evolution of Earth's tectonic carbon conveyor belt.

Concealed deep beneath the oceans is a carbon conveyor belt, propelled by plate tectonics. Our understanding of its modern functioning is underpinned by direct observations, but its variability through time has been poorly quantified. Here we reconstruct oceanic plate carbon reservoirs and track the fate of subducted carbon using thermodynamic modelling. In the Mesozoic era, 250 to 66 million years ago, plate tectonic processes had a pivotal role in driving climate change. Triassic-Jurassic period cooling correlates with a reduction in solid Earth outgassing, whereas Cretaceous period greenhouse conditions can be linked to a doubling in outgassing, driven by high-speed plate tectonics. The associated 'carbon subduction superflux' into the subcontinental mantle may have sparked North American diamond formation. In the Cenozoic era, continental collisions slowed seafloor spreading, reducing tectonically driven outgassing, while deep-sea carbonate sediments emerged as the Earth's largest carbon sink. Subduction and devolatilization of this reservoir beneath volcanic arcs led to a Cenozoic increase in carbon outgassing, surpassing mid-ocean ridges as the dominant source of carbon emissions 20 million years ago. An increase in solid Earth carbon emissions during Cenozoic cooling requires an increase in continental silicate weathering flux to draw down atmospheric carbon dioxide, challenging previous views and providing boundary conditions for future carbon cycle models.

The land-to-ocean loops of the global carbon cycle.

Carbon storage by the ocean and by the land is usually quantified separately, and does not fully take into account the land-to-ocean transport of carbon through inland waters, estuaries, tidal wetlands and continental shelf waters-the 'land-to-ocean aquatic continuum' (LOAC). Here we assess LOAC carbon cycling before the industrial period and perturbed by direct human interventions, including climate change. In our view of the global carbon cycle, the traditional 'long-range loop', which carries carbon from terrestrial ecosystems to the open ocean through rivers, is reinforced by two 'short-range loops' that carry carbon from terrestrial ecosystems to inland waters and from tidal wetlands to the open ocean. Using a mass-balance approach, we find that the pre-industrial uptake of atmospheric carbon dioxide by terrestrial ecosystems transferred to the ocean and outgassed back to the atmosphere amounts to 0.65 ± 0.30 petagrams of carbon per year (±2 sigma). Humans have accelerated the cycling of carbon between terrestrial ecosystems, inland waters and the atmosphere, and decreased the uptake of atmospheric carbon dioxide from tidal wetlands and submerged vegetation. Ignoring these changing LOAC carbon fluxes results in an overestimation of carbon storage in terrestrial ecosystems by 0.6 ± 0.4 petagrams of carbon per year, and an underestimation of sedimentary and oceanic carbon storage. We identify knowledge gaps that are key to reduce uncertainties in future assessments of LOAC fluxes.

Cyclic evolution of phytoplankton forced by changes in tropical seasonality.

Although the role of Earth's orbital variations in driving global climate cycles has long been recognized, their effect on evolution is hitherto unknown. The fossil remains of coccolithophores, a key calcifying phytoplankton group, enable a detailed assessment of the effect of cyclic orbital-scale climate changes on evolution because of their abundance in marine sediments and the preservation of their morphological adaptation to the changing environment1,2. Evolutionary genetic analyses have linked broad changes in Pleistocene fossil coccolith morphology to species radiation events3. Here, using high-resolution coccolith data, we show that during the last 2.8 million years the morphological evolution of coccolithophores was forced by Earth's orbital eccentricity with rhythms of around 100,000 years and 405,000 years-a distinct spectral signature to that of coeval global climate cycles4. Simulations with an Earth System Model5 coupled with an ocean biogeochemical model6 show a strong eccentricity modulation of the seasonal cycle, which we suggest directly affects the diversity of ecological niches that occur over the annual cycle in the tropical ocean. Reduced seasonality in surface ocean conditions favours species with mid-size coccoliths, increasing coccolith carbonate export and burial; whereas enhanced seasonality favours a larger range of coccolith sizes and reduced carbonate export. We posit that eccentricity pacing of phytoplankton evolution contributed to the strong 405,000-year cyclicity that is seen in global carbon cycle records.

Decoupling of respiration rates and abundance in marine prokaryoplankton.

The ocean-atmosphere exchange of CO2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton)1-3, their respiration usually is measured in bulk and treated as a 'black box' in global biogeochemical models4; this limits the mechanistic understanding of the global carbon cycle. Here, using a technology for integrated phenotype analyses and genomic sequencing of individual microbial cells, we show that cell-specific respiration rates differ by more than 1,000× among prokaryoplankton genera. The majority of respiration was found to be performed by minority members of prokaryoplankton (including the Roseobacter cluster), whereas cells of the most prevalent lineages (including Pelagibacter and SAR86) had extremely low respiration rates. The decoupling of respiration rates from abundance among lineages, elevated counts of proteorhodopsin transcripts in Pelagibacter and SAR86 cells and elevated respiration of SAR86 at night indicate that proteorhodopsin-based phototrophy3,5-7 probably constitutes an important source of energy to prokaryoplankton and may increase growth efficiency. These findings suggest that the dependence of prokaryoplankton on respiration and remineralization of phytoplankton-derived organic carbon into CO2 for its energy demands and growth may be lower than commonly assumed and variable among lineages.

The three major axes of terrestrial ecosystem function.

The leaf economics spectrum1,2 and the global spectrum of plant forms and functions3 revealed fundamental axes of variation in plant traits, which represent different ecological strategies that are shaped by the evolutionary development of plant species2. Ecosystem functions depend on environmental conditions and the traits of species that comprise the ecological communities4. However, the axes of variation of ecosystem functions are largely unknown, which limits our understanding of how ecosystems respond as a whole to anthropogenic drivers, climate and environmental variability4,5. Here we derive a set of ecosystem functions6 from a dataset of surface gas exchange measurements across major terrestrial biomes. We find that most of the variability within ecosystem functions (71.8%) is captured by three key axes. The first axis reflects maximum ecosystem productivity and is mostly explained by vegetation structure. The second axis reflects ecosystem water-use strategies and is jointly explained by variation in vegetation height and climate. The third axis, which represents ecosystem carbon-use efficiency, features a gradient related to aridity, and is explained primarily by variation in vegetation structure. We show that two state-of-the-art land surface models reproduce the first and most important axis of ecosystem functions. However, the models tend to simulate more strongly correlated functions than those observed, which limits their ability to accurately predict the full range of responses to environmental changes in carbon, water and energy cycling in terrestrial ecosystems7,8.

The contribution of insects to global forest deadwood decomposition.

The amount of carbon stored in deadwood is equivalent to about 8 per cent of the global forest carbon stocks1. The decomposition of deadwood is largely governed by climate2-5 with decomposer groups-such as microorganisms and insects-contributing to variations in the decomposition rates2,6,7. At the global scale, the contribution of insects to the decomposition of deadwood and carbon release remains poorly understood7. Here we present a field experiment of wood decomposition across 55 forest sites and 6 continents. We find that the deadwood decomposition rates increase with temperature, and the strongest temperature effect is found at high precipitation levels. Precipitation affects the decomposition rates negatively at low temperatures and positively at high temperatures. As a net effect-including the direct consumption by insects and indirect effects through interactions with microorganisms-insects accelerate the decomposition in tropical forests (3.9% median mass loss per year). In temperate and boreal forests, we find weak positive and negative effects with a median mass loss of 0.9 per cent and -0.1 per cent per year, respectively. Furthermore, we apply the experimentally derived decomposition function to a global map of deadwood carbon synthesized from empirical and remote-sensing data, obtaining an estimate of 10.9 ± 3.2 petagram of carbon per year released from deadwood globally, with 93 per cent originating from tropical forests. Globally, the net effect of insects may account for 29 per cent of the carbon flux from deadwood, which suggests a functional importance of insects in the decomposition of deadwood and the carbon cycle.