Remineralization of organic matter by heterotrophic organisms regulates the biological sequestration of carbon, thereby mediating atmospheric CO2. While surface nutrient supply impacts the elemental ratios of primary production, stoichiometric control by remineralization remains unclear. Here we develop a mechanistic description of remineralization and its stoichiometry in a marine microbial ecosystem model. The model simulates the observed elemental plasticity of phytoplankton and the relatively constant, lower C:N of heterotrophic biomass. In addition, the model captures the observed decreases in DOC:DON and the C:N remineralization ratio with depth for more labile substrates, which are driven by a switch in the dominant source of labile DOM from phytoplankton to heterotrophic biomass. Only a model version with targeted remineralization of N-rich components is able to simulate the observed profiles of preferential remineralization of DON relative to DOC and the elevated C:N of bulk DOM. The model suggests that more labile substrates are associated with C-limited heterotrophic growth and not with preferential remineralization, while more recalcitrant substrates are associated with growth limited by processing rates and with preferential remineralization. The resulting patterns of variable remineralization stoichiometry mediate the extent to which a proportional increase in carbon production resulting from changes in phytoplankton stoichiometry can increase the efficiency of the biological pump. Results emphasize the importance of understanding the physiology of both phytoplankton and heterotrophs for anticipating changes in biologically driven ocean carbon storage.

Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about how microbial populations will evolve due to global change-driven shifts in ocean dynamics. Understanding adaptive timescales is critical where long-term trends (e.g. warming) are coupled to shorter-term advection dynamics that move organisms rapidly between ecoregions. Here we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria ( and {beta}) were identified that relate physical and biological timescales and determine the timing and nature of adaptation. Genetic adaptation was impeded in highly variable regimes (<1) but promoted in more stable environments (>1). An evolutionary trade-off emerged where greater short-term transgenerational effects (low-{beta}-strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-{beta}-strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results suggest that organisms with faster growth rates are better positioned to adapt to rapidly changing ocean conditions and that more variable environments will favor a bet-hedging, low-{beta}-strategy. Understanding the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.

Anoxic marine zones (AMZs) are host to anaerobic metabolisms that drive losses of bioavailable nitrogen from the ocean. The discovery of active nitrite-oxidising bacteria (NOB), long thought to be obligately aerobic, in AMZs has altered our perception of how nitrogen cycles in these oxygen-deficient waters. Yet, why NOB succeed in AMZs remains unclear. Here, we show that obligately aerobic NOB can thrive alongside aerobic microheterotrophs in AMZs via infrequent intrusions of oxygen. Ecological theory, biogeochemical modelling and metagenome-based maximum growth rate estimates suggest that NOB are opportunists that take advantage of periodic oxygen intrusions to rapidly accumulate biomass. Rather than harsh, AMZs prone to oxygen intrusions appear optimal for NOB, whose abundance and activity peaks in a goldilocks zone of periodic oxygen and high nitrite supply. Our results recast the intermediate disturbance hypothesis to AMZs and highlight how the nitrogen cycle relies on dynamic coexistence of aerobic and anaerobic metabolisms.

Nitrous oxide (N2O), a potent greenhouse gas in the atmosphere, is produced mostly from aquatic ecosystems, to which algae substantially contribute. However, mechanisms of N2O production by photosynthetic organisms are poorly described. Here, we show that the green microalga Chlamydomonas reinhardtii reduces NO into N2O using the photosynthetic electron transport. Through the study of C. reinhardtii mutants deficient in flavodiiron proteins (FLVs) or in a cytochrome p450 (CYP55), we show that FLVs contribute to NO reduction in the light, while CYP55 operates in the dark. Furthermore, NO reduction by both pathways is restricted to Chlorophytes, organisms particularly abundant in ocean N2O-producing hotspots. Our results provide a mechanistic understanding of N2O production in eukaryotic phototrophs and represent an important step toward a comprehensive assessment of greenhouse gas emission by aquatic ecosystems.One sentence summaryGreen microalgae produce N2O using flavodiiron proteins in the light and a cytochrome P450 NO reductase in the dark.

Photosynthesis in cyanobacteria, green algae, and basal land plants is protected against excess reducing pressure on the photosynthetic chain by flavodiiron proteins (FLV) that dissipate photosynthetic electrons by reducing O2. In these organisms, the genes encoding FLV are always conserved in the form of a pair of two-type isozymes (FLVA and FLVB) that are believed to function in O2 photo-reduction as a heterodimer. While coral symbionts (dinoflagellates of the family Symbiodiniaceae) are the only algae to harbor FLV in photosynthetic red plastid lineage, only one gene is found in transcriptomes and its role and activity remain unknown. Here, we characterized the FLV genes in Symbiodiniaceae and found that its coding region is composed of tandemly repeated FLV sequences. By measuring the O2-dependent electron flow and P700 oxidation, we suggest that this atypical FLV is active in vivo. Based on the amino-acid sequence alignment and the phylogenetic analysis, we conclude that in coral symbionts, the gene pair for FLVA and FLVB have been fused to construct one coding region for a hybrid enzyme, which presumably occurred when or after both genes were inherited from basal green algae to the dinoflagellate. Immunodetection suggested the FLV polypeptide to be cleaved by a post-translational mechanism, adding it to the rare cases of polycistronic genes in eukaryotes. Our results demonstrate that FLV are active in coral symbionts with genomic arrangement that is unique to these species. The implication of these unique features on their symbiotic living environment is discussed.

Photosynthetic organisms use sunlight as the primary energy source to fix CO2. However, in the environment, light energy fluctuates rapidly and often exceeds saturating levels for periods ranging from seconds to hours, which can lead to detrimental effects for cells. Safe dissipation of excess light energy occurs primarily by non-photochemical quenching (NPQ) processes. In the model green microalga Chlamydomonas reinhardtii, photoprotective NPQ is mostly mediated by pH-sensing light-harvesting complex stress-related (LHCSR) proteins and the redistribution of light-harvesting antenna proteins between the photosystems (state transition). Although each component underlying NPQ has been documented, their relative contributions to the dynamic functioning of NPQ under fluctuating light conditions remains unknown. Here, by monitoring NPQ throughout multiple high light-dark cycles with fluctuation periods ranging from 1 to 10 minutes, we show that the dynamics of NPQ depend on the frequency of light fluctuations. Mutants impaired in the accumulation of LHCSRs (npq4, lhcsr1, and npq4lhcsr1) showed significantly less quenching during illumination, demonstrating that LHCSR proteins are responsible for the majority of NPQ during repetitive exposure to high light fluctuations. Activation of NPQ was also observed during the dark phases of light fluctuations, and this was exacerbated in mutants lacking LHCSRs. By analyzing 77K chlorophyll fluorescence spectra and chlorophyll fluorescence lifetimes and yields in a mutant impaired in state transition, we show that this phenomenon arises from state transition. Finally, we quantified the contributions of LHCSRs and state transition to the overall NPQ amplitude and dynamics for all light periods tested and compared those with cell growth under various periods of fluctuating light. These results highlight the dynamic functioning of photoprotection under light fluctuations and open a new way to systematically characterize the photosynthetic response to an ever-changing light environment. One sentence summary: The roles of LHCSR and STT7 in NPQ vary with the light fluctuation period and duration of light fluctuation.

Photosynthetic organisms have developed sophisticated strategies to fine-tune light energy conversion to meet the metabolic demand, thereby optimizing growth in fluctuating light environments. Although mechanisms such as energy dissipation, photosynthetic control, or the photosystem II (PSII) damage and repair have been widely studied, little is known about the regulation of protein synthesis capacity during light acclimation. By screening a Chlamydomonas reinhardtii insertional mutant library using chlorophyll fluorescence imaging, we isolated a high chlorophyll fluorescence mutant (hf0) defected in a gene encoding a putative plastid targeted DEAD-box RNA helicase called CreRH22. CreRH22 is rapidly induced upon illumination and belongs to the GreenCut, a set of proteins specific to photosynthetic organisms. While photosynthesis is slightly affected in the mutant under low light (LL), exposure to high light (HL) induces a marked decrease in both PSII and PSI, and a strong alteration of the light-induced gene expression pattern. These effects are explained by the inability of hf0 to increase plastid ribosome amounts under HL. We conclude that CreRH22, by promoting ribosomal RNA precursor maturation in a light-dependent manner, enables the assembly of extra ribosomes required to synthesize photosystem subunits at a higher rate, a critical step in the acclimation of algae to HL.

The maize female gametophyte is comprised of four cell types: two synergids, an egg cell, a central cell, and a variable number of antipodal cells. In maize, these cells are produced after three rounds of free-nuclear divisions followed by cellularization, differentiation, and proliferation of the antipodal cells. Cellularization of the eight-nucleate syncytium produces seven cells with two polar nuclei in the central cell. Nuclear localization is tightly controlled in the embryo sac as evidenced by the regular, stereotypical position of the nuclei in all syncytial stages of female gametophyte development. This leads to precise allocation of the nuclei into the cells upon cellularization. Nuclear positioning within the syncytium is highly correlated with their identity after cellularization. Two mutants are described with extra polar nuclei, abnormal antipodal cell morphology, and reduced antipodal cell number, which is correlated with a frequent loss of auxin signaling in the antipodal cell cluster. Mutations in one of these genes, indeterminate gametophyte2 encoding a MICROTUBULE ASSOCIATED PROTEIN65-3 homolog, shows a requirement for MAP65-3 in cellularization of the syncytial embryo sac and that the identity of the nuclei in the syncytial female gametophyte can be changed very late before cellularization.

Photosynthetic algae cope with suboptimal levels of light and CO2. In low CO2 and excess light, the green alga Chlamydomonas reinhardtii activates a CO2 Concentrating Mechanism (CCM) and photoprotection; the latter is mediated by LHCSR1/3 and PSBS. How light and CO2 signals converge to regulate photoprotective responses remains unclear. Here we show that excess light activates expression of photoprotection-and CCM-related genes and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3 and CCM genes while stabilizing the LHCSR1 protein. We also show that CIA5, which controls CCM genes, is a major regulator of photoprotection, elevating LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 accumulation. Our work emphasizes the importance of CO2 in regulating photoprotection and the CCM, demonstrating that the impact of light on photoprotection is often indirect and reflects intracellular CO2 levels.

In nature, photosynthetic organisms are exposed to different light spectra and intensities depending on the time of day and atmospheric and environmental conditions. When photosynthetic cells absorb excess light, they induce non-photochemical quenching to avoid photo-damage and trigger expression of ‘photoprotective’ genes. In this work, we used the green alga Chlamydomonas reinhardtii to assess the impact of light intensity, light quality, wavelength, photosynthetic electron transport and CO2 on induction of the ‘photoprotective’ genes (LHCSR1, LHCSR3 and PSBS) during dark-to-light transitions. Induction (mRNA accumulation) occurred at very low light intensity, was independently modulated by blue and UV-B radiation through specific photoreceptors, and only LHCSR3 was strongly controlled by CO2 levels through a putative enhancer function of CIA5, a transcription factor that controls genes of the carbon concentrating mechanism. We propose a model that integrates inputs of independent signaling pathways and how they may help the cells anticipate diel conditions and survive in a dynamic light environment.