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Microalgae can contribute to food security through the sustainable production of proteins and lipids, which are required to meet population growth and address environmental challenges.Cellular agriculture is developing with emerging bioprocesses based on solar energy, photovoltaics, H2, C1 carbon sources, and sugar as feedstocks.Different trophic modes – autotrophy, heterotrophy, and mixotrophy – have been successfully explored for microalgae.The production of microalgae has tripled in the last 5 years.The genetic toolbox for industrially relevant phototrophic strains expanded tremendously in the last 5 years. The urge for food security and sustainability has advanced the field of microalgal biotechnology. Microalgae are microorganisms able to grow using (sun)light, fertilizers, sugars, CO2, and seawater. They have high potential as a feedstock for food, feed, energy, and chemicals. Microalgae grow faster and have higher areal productivity than plant crops, without competing for agricultural land and with 100% efficiency uptake of fertilizers. In comparison with bacterial, fungal, and yeast single-cell protein production, based on hydrogen or sugar, microalgae show higher land-use efficiency. New insights are provided regarding the potential of microalgae replacing soy protein, fish oil, and palm oil and being used as cell factories in modern industrial biotechnology to produce designer feed, recombinant proteins, biopharmaceuticals, and vaccines.

Natural and anthropogenic wetlands are major sources of the atmospheric greenhouse gas methane.Methane emissions from wetlands are mitigated by methanotrophic bacteria at the oxic–anoxic interface, a zone of intense redox cycling of carbon, sulfur, and nitrogen compounds. Here, we report on the isolation of an aerobic methanotrophic bacterium, ‘Methylovirgula thiovorans’ strain HY1, which possesses metabolic capabilities never before found in any methanotroph. Most notably, strain HY1 is the first bacterium shown to aerobically oxidize both methane and reduced sulfur compounds for growth. Genomic and proteomic analyses showed that soluble methane monooxygenase and XoxF-type alcohol dehydrogenases are responsible for methane and methanol oxidation, respectively. Various pathways for respiratory sulfur oxidation were present, including the Sox—rDsr pathway and the S₄I system. Strain HY1 employed the Calvin—Benson–Bassham cycle for CO₂ fixation during chemolithoautotrophic growth on reduced sulfur compounds. Proteomic and microrespirometry analyses showed that the metabolic pathways for methane and thiosulfate oxidation were induced in the presence of the respective substrates. Methane and thiosulfate could therefore be independently or simultaneously oxidized. The discovery of this versatile bacterium demonstrates that methanotrophy and thiotrophy are compatible in a single microorganism and underpins the intimate interactions of methane and sulfur cycles in oxic—anoxic interface environments.

Mixotrophy, the combination of autotrophic and heterotrophic nutrition, is a common trophic strategy among unicellular eukaryotes in the ocean. There are a number of hypotheses about the conditions that select for mixotrophy, and field studies have documented the prevalence of mixotrophy in a range of environments. However, there is currently little evidence for how mixotrophy varies across environmental gradients, and whether empirical patterns support theoretical predictions. Here I synthesize experiments that have quantified the abundance of phototrophic, mixotrophic, and heterotrophic nanoflagellates, to ask whether there are broad patterns in the prevalence of mixotrophy (relative to pure autotrophy and heterotrophy), and to ask whether observed patterns are consistent with a trait-based model of trophic strategies. The data suggest that mixotrophs increase in abundance at lower latitudes, while autotrophs and heterotrophs do not, and that this may be driven by increased light availability. Both mixotrophs and autotrophs increase greatly in productive coastal environments, while heterotrophs increase only slightly. These patterns are consistent with a model of resource competition in which nutrients and carbon can both limit growth and mixotrophs experience a trade-off in allocating biomass to phagotrophy vs. autotrophic functions. Importantly, mixotrophy is selected for under a range of conditions even when mixotrophs experience a penalty for using a generalist trophic strategy, due to the synergy between photosynthetically derived carbon and prey-derived nutrients. For this reason mixotrophy is favored relative to specialist strategies by increased irradiance, while at the same time increased nutrient supply increases the competitive ability of mixotrophs against heterotrophs.

Mixotrophy, a physiological trait combining autotrophy and heterotrophy in one organism, significantly contributes to energy and matter transfer in aquatic ecosystems. However, understanding how environmental factors influence mixoplankton success across freshwater ecosystems has been uncertain. The grand écart hypothesis (GEH) posits that light and nutrient availability are key components of mixotrophs' niche, suggesting that ecosystem properties determine opposing gradients of light and nutrients, creating environmental filtering for mixotrophs. We hypothesized that ecosystem size, a property of lake ecosystems, mediates the prevalence of patterns and control mechanisms predicted by the GEH on mixoplankton relative biomass (MRB). Using data from 98 tropical lakes, we demonstrated that lake size mediates the inverse relationship between light and nutrient availability across ecosystems. Larger lakes have more light but low nutrients, while smaller lakes have more nutrients but greater shading. Light availability better explains MRB in small lakes, and nutrients better explain MRB in large lakes, with MRB values being higher in small lakes, with secondary influence from zooplankton herbivory. Our results validate the GEH as a significant framework for explaining patterns and control mechanisms of mixoplankton across tropical lakes. This study highlights the significance of lake size as an ecosystem property that generates opposing light and nutrient gradients, further emphasizing its importance for understanding mechanisms regulating freshwater phytoplankton community structure and functioning. Integrating lake size within the conceptual framework of the GEH could aid in explaining mixoplankton success over macroecological scales.

The major bottleneck in commercializing biofuels and other commodities produced by microalgae is the high cost associated with phototrophic cultivation. Improving microalgal productivities could be a solution to this problem. Synthetic biology methods have recently been used to engineer the downstream production pathways in several microalgal strains. However, engineering upstream photosynthetic and carbon fixation metabolism to enhance growth, productivity, and yield has barely been explored in microalgae. We describe strategies to improve the generation of reducing power from light, as well as to improve the assimilation of CO2 by either the native Calvin cycle or synthetic alternatives. Overall, we are optimistic that recent technological advances will prompt long-awaited breakthroughs in microalgal research. The high cost of microalgal cultivation has hindered exploitation of their advantages for sustainable production of green chemicals and biomass. Nevertheless, recent advances in the field of synthetic biology could help to overcome the associated bottlenecks.Improving reducing power generation and carbon influx will be crucial for attaining an overall improvement in microalgal productivity.Enhancing light absorption, in conjunction with techniques to swiftly channel electrons through the electron transport chain, could enhance the generation of reducing power.The Calvin–Benson–Bassham (CBB) cycle might not be the best CO2 fixation pathway, and other natural and synthetic pathways may outperform the CBB cycle. However, implementing these entire pathways in new hosts will be very challenging.Mixotrophic cultivation and microbial electrosynthesis could be implemented as an additional source of energy and carbon to improve microalgal productivity.

Mycorrhizal fungi are central to the biology of land plants. However, to what extent mycorrhizal shifts – broad evolutionary transitions in root-associated fungal symbionts – are related to changes in plant trophic modes remains poorly understood. We built a comprehensive DNA dataset of Orchidaceae fungal symbionts and a dated plant molecular phylogeny to test the hypothesis that shifts in orchid trophic modes follow a stepwise pattern, from autotrophy over partial mycoheterotrophy (mixotrophy) to full mycoheterotrophy, and that these shifts are accompanied by switches in fungal symbionts. We estimate that at least 17 independent shifts from autotrophy towards full mycoheterotrophy occurred in orchids, mostly through an intermediate state of partial mycoheterotrophy. A wide range of fungal partners was inferred to occur in the roots of the common ancestor of this family, including ‘rhizoctonias’, ectomycorrhizal, and wood- or litter-decaying saprotrophic fungi. Phylogenetic hypothesis tests further show that associations with ectomycorrhizal or saprotrophic fungi were most likely a prerequisite for evolutionary shifts towards full mycoheterotrophy. We show that shifts in trophic mode often coincided with switches in fungal symbionts, suggesting that the loss of photosynthesis selects for different fungal communities in orchids. We conclude that changes in symbiotic associations and ecophysiological traits are tightly correlated throughout the diversification of orchids.

Ammonia-oxidizing archaea (AOA), that is, members of the Thaumarchaeota phylum, occur ubiquitously in the environment and are of major significance for global nitrogen cycling. However, controls on cell growth and organic carbon assimilation by AOA are poorly understood. We isolated an ammonia-oxidizing archaeon (designated strain DDS1) from seawater and used this organism to study the physiology of ammonia oxidation. These findings were confirmed using four additional Thaumarchaeota strains from both marine and terrestrial habitats. Ammonia oxidation by strain DDS1 was enhanced in coculture with other bacteria, as well as in artificial seawater media supplemented with α-keto acids (e.g., pyruvate, oxaloacetate). α-Keto acid-enhanced activity of AOA has previously been interpreted as evidence of mixotrophy. However, assays for heterotrophic growth indicated that incorporation of pyruvate into archaeal membrane lipids was negligible. Lipid carbon atoms were, instead, derived from dissolved inorganic carbon, indicating strict autotrophic growth. α-Keto acids spontaneously detoxify H₂O₂ via a nonenzymatic decarboxylation reaction, suggesting a role of α-keto acids as H₂O₂ scavengers. Indeed, agents that also scavenge H₂O₂, such as dimethylthiourea and catalase, replaced the α-keto acid requirement, enhancing growth of strain DDS1. In fact, in the absence of α-keto acids, strain DDS1 and other AOA isolates were shown to endogenously produce H₂O₂ (up to ∼4.5 μM), which was inhibitory to growth. Genomic analyses indicated catalase genes are largely absent in the AOA. Our results indicate that AOA broadly feature strict autotrophic nutrition and implicate H₂O₂ as an important factor determining the activity, evolution, and community ecology of AOA ecotypes.

Mixotrophic plankton, which combine the uptake of inorganic resources and the ingestion of living prey, are ubiquitous in marine ecosystems, but their integrated biogeochemical impacts remain unclear. We address this issue by removing the strict distinction between phytoplankton and zooplankton from a global model of the marine plankton food web. This simplification allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry, relative to a system in which autotrophy and heterotrophy are mutually exclusive. Mixotrophy enhances the transfer of biomass to larger sizes classes further up the food chain, leading to an approximately threefold increase in global mean organism size and an ∼35% increase in sinking carbon flux.

Intricate networks of single-celled eukaryotes (protists) dominate carbon flow in the ocean. Their growth, demise, and interactions with other microorganisms drive the fluxes of biogeochemical elements through marine ecosystems. Mixotrophic protists are capable of both photosynthesis and ingestion of prey and are dominant components of open-ocean planktonic communities. Yet the role of mixotrophs in elemental cycling is obscured by their capacity to act as primary producers or heterotrophic consumers depending on factors that remain largely uncharacterized. Here, we develop and apply a machine learning model that predicts the in situ trophic mode of aquatic protists based on their patterns of gene expression. This approach leverages a public collection of protist transcriptomes as a training set to identify a subset of gene families whose transcriptional profiles predict trophic mode. We applied our model to nearly 100 metatranscriptomes obtained during two oceanographic cruises in the North Pacific and found community-level and population-specific evidence that abundant open-ocean mixotrophic populations shift their predominant mode of nutrient and carbon acquisition in response to natural gradients in nutrient supply and sea surface temperature. Metatranscriptomic data from ship-board incubation experiments revealed that abundant mixotrophic prymnesiophytes from the oligotrophic North Pacific subtropical gyre rapidly remodeled their transcriptome to enhance photosynthesis when supplied with limiting nutrients. Coupling this approach with experiments designed to reveal the mechanisms driving mixotroph physiology provides an avenue toward understanding the ecology of mixotrophy in the natural environment.

Diatoms are prominent marine microalgae, interesting not only from an ecological point of view, but also for their possible use in biotechnology applications. They can be cultivated in phototrophic conditions, using sunlight as the sole energy source. Some diatoms, however, can also grow in a mixotrophic mode, wherein both light and external reduced carbon contribute to biomass accumulation. In this study, we investigated the consequences of mixotrophy on the growth and metabolism of the pennate diatom Phaeodactylum tricornutum, using glycerol as the source of reduced carbon. Transcriptomics, metabolomics, metabolic modelling and physiological data combine to indicate that glycerol affects the central-carbon, carbon-storage and lipid metabolism of the diatom. In particular, provision of glycerol mimics typical responses of nitrogen limitation on lipid metabolism at the level of triacylglycerol accumulation and fatty acid composition. The presence of glycerol, despite provoking features reminiscent of nutrient limitation, neither diminishes photosynthetic activity nor cell growth, revealing essential aspects of the metabolic flexibility of these microalgae and suggesting possible biotechnological applications of mixotrophy.This article is part of the themed issue 'The peculiar carbon metabolism in diatoms'.