Modelling phytoplankton-virus interactions: phytoplankton blooms and lytic virus transmission.

A dynamic reaction-diffusion model of four variables is proposed to describe the spread of lytic viruses among phytoplankton in a poorly mixed aquatic environment. The basic ecological reproductive index for phytoplankton invasion and the basic reproduction number for virus transmission are derived to characterize the phytoplankton growth and virus transmission dynamics. The theoretical and numerical results from the model show that the spread of lytic viruses effectively controls phytoplankton blooms. This validates the observations and experimental results of Emiliana huxleyi-lytic virus interactions. The studies also indicate that the lytic virus transmission cannot occur in a low-light or oligotrophic aquatic environment.

Effects of temperature and nitrogen sources on physiological performance of the coccolithophore Emiliania huxleyi.

Both temperature and nutrient levels are rising in worldwide ocean ecosystems, and they strongly influence biological responses of phytoplankton. However, few studies have addressed the interactive effects of temperature and nitrogen sources on physiological performance of the coccolithophore Emiliania huxleyi. In this study, we evaluated algal growth, photosynthesis and respiration, elemental composition, enzyme activity, and calcification under a matrix of two temperatures gradients (ambient temperature 20 °C and high temperature 24 °C) and two nitrogen sources (nitrate (NO3-) and ammonium (NH4+)). When the algae was cultured with NO3- medium, high temperature reduced algal photosynthesis and nitrate reductase activity, but it did not change other indicators significantly relative to ambient temperature. In addition, E. huxleyi preferred NO3- as the growth medium, whereas NH4+ had negative effects on physiological parameters. In the NH4+ medium, the growth rate, photosynthesis and photosynthetic rate, nitrate reductase activity, and particulate organic carbon and particulate organic nitrogen production rate of the algae decreased as temperature increased. Conversely, high temperature increased cellular particulate organic carbon, cellular particulate organic nitrogen, and particulate inorganic carbon levels. In summary, our findings indicate that the distribution and abundance of microalgae could be greatly affected under warming ocean temperature and different nutrient conditions.

Ocean acidification affects physiology of coccolithophore Emiliania huxleyi and weakens its mechanical resistance to copepods.

The effects of ocean acidification (OA) on coccolithophore's photosynthesis, calcification rates, and growth have been extensively studied. However, how the intracellular Ca2+, mechanical properties and chemical composition of the coccoliths are affected by OA have not yet been investigated. This study tries to fill these gaps using Emiliania huxleyi as a model coccolithophore. When the seawater pCO2 increased from 400 µatm to 1200 µatm, the intracellular Ca2+ and coccolith area were reduced by 66% and 36%, respectively. Single-cell mapping by atomic force microscopy revealed that the modulus and hardness of coccolith decreased from 23.6 ± 0.2 GPa to 12.0 ± 5.5 GPa and from 0.53 ± 0.15 GPa to 0.20 ± 0.06 GPa, respectively. Additionally, the proportional organic matter and silicon in the coccolith surfaces increased with pCO2. The copepods Acartia pacifica fed on more E. huxleyi grown at higher pCO2. Our study implies that OA could change coccolithophore's competitive interactions with other phytoplankton and ultimately influence carbon export to the deep ocean.

Regulation of photosynthetic and hemolytic activity of Phaeocystis globosa under different light spectra.

Phaeocystis globosa frequently proliferates in eutrophic waters and forms ichthyotoxic algal blooms that cause massive fish mortalities in marine ecosystems. One of the ichthyotoxic metabolites was identified as the glycolipid-like hemolytic toxin, reported to be initiated under light conditions. However, the association between hemolytic activity (HA) and photosynthesis of P. globosa remained unclear. Light spectra (blue, red, green, and white) and 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) were selected as the stressors to stimulate the hemolytic response of P. globosa in relation to the light and dark photosynthesis reaction. Hemolytic activity in P. globosa was sensitive to the light spectrum as it decreased from 93% to nearly undetectable (1.6%) within 10 min of transfer from red (630 nm) to green light (520 nm). This indicates that the vertical transformation of P. globosa from deep to surface waters (dominated by green light and all light spectra, respectively) may drive the hemolytic response in coastal waters. However, regulation of photosynthetic electron transfer in the light reaction of P. globosa was excluded by the evidence of inconsistent response of HA to photosynthetic activity. The biosynthesis of HA may interfere with the pathway of photopigments diadinoxanthin or fucoxanthin, and the metabolism of three- and five-carbon sugars (GAP and Ru5P, respectively), which ultimately lead to changes in the alga's hemolytic carbohydrate metabolism.

Unexpected silicon localization in calcium carbonate exoskeleton of cultured and fossil coccolithophores.

Coccolithophores, marine calcifying phytoplankton, are important primary producers impacting the global carbon cycle at different timescales. Their biomineral structures, the calcite containing coccoliths, are among the most elaborate hard parts of any organism. Understanding the morphogenesis of coccoliths is not only relevant in the context of coccolithophore eco-physiology but will also inform biomineralization and crystal design research more generally. The recent discovery of a silicon (Si) requirement for crystal shaping in some coccolithophores has opened up a new avenue of biomineralization research. In order to develop a mechanistic understanding of the role of Si, the presence and localization of this chemical element in coccoliths needs to be known. Here, we document for the first time the uneven Si distribution in Helicosphaera carteri coccoliths through three synchrotron-based techniques employing X-ray Fluorescence and Infrared Spectromicroscopy. The enrichment of Si in specific areas of the coccoliths point to a targeted role of this element in the coccolith formation. Our findings mark a key step in biomineralization research because it opens the door for a detailed mechanistic understanding of the role Si plays in shaping coccolith crystals.

High-CO2 Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance.

The coccolithophore Emiliania huxleyi shows a variety of responses to ocean acidification (OA) and to high-CO2 concentrations, but there is still controversy on differentiating between these two factors when using different strains and culture methods. A heavily calcified type A strain isolated from the Norwegian Sea was selected and batch cultured in order to understand whether acclimation to OA was mediated mainly by CO2 or H+, and how it impacted cell growth performance, calcification, and physiological stress management. Emiliania huxleyi responded differently to each acidification method. CO2-enriched aeration (1200 µatm, pH 7.62) induced a negative effect on the cells when compared to acidification caused by decreasing pH alone (pH 7.60). The growth rates of the coccolithophore were more negatively affected by high pCO2 than by low pH without CO2 enrichment with respect to the control (400 µatm, pH 8.1). High CO2 also affected cell viability and promoted the accumulation of reactive oxygen species (ROS), which was not observed under low pH. This suggests a possible metabolic imbalance induced by high CO2 alone. In contrast, the affinity for carbon uptake was negatively affected by both low pH and high CO2. Photochemistry was only marginally affected by either acidification method when analysed by PAM fluorometry. The POC and PIC cellular quotas and the PIC:POC ratio shifted along the different phases of the cultures; consequently, calcification did not follow the same pattern observed in cell stress and growth performance. Specifically, acidification by HCl addition caused a higher proportion of severely deformed coccoliths, than CO2 enrichment. These results highlight the capacity of CO2 rather than acidification itself to generate metabolic stress, not reducing calcification.

Interactions between Filter-Feeding Bivalves and Toxic Diatoms: Influence on the Feeding Behavior of Crassostrea gigas and Pecten maximus and on Toxin Production by Pseudo-nitzschia.

Among Pseudo-nitzschia species, some produce the neurotoxin domoic acid (DA), a source of serious health problems for marine organisms. Filter-feeding organisms-e.g., bivalves feeding on toxigenic Pseudo-nitzschia spp.-are the main vector of DA in humans. However, little is known about the interactions between bivalves and Pseudo-nitzschia. In this study, we examined the interactions between two juvenile bivalve species-oyster (Crassostrea gigas) and scallop (Pecten maximus)-and two toxic Pseudo-nitzschia species-P. australis and P. fraudulenta. We characterized the influence of (1) diet composition and the Pseudo-nitzschia DA content on the feeding rates of oysters and scallops, and (2) the presence of bivalves on Pseudo-nitzschia toxin production. Both bivalve species fed on P. australis and P. fraudulenta. However, they preferentially filtered the non-toxic Isochrysis galbana compared to Pseudo-nitzschia. The presence of the most toxic P. australis species resulted in a decreased clearance rate in C. gigas. The two bivalve species accumulated DA in their tissues (up to 0.35 × 10-3 and 5.1 × 10-3 µg g-1 for C. gigas and P. maximus, respectively). Most importantly, the presence of bivalves induced an increase in the cellular DA contents of both Pseudo-nitzschia species (up to 58-fold in P. fraudulenta in the presence of C. gigas). This is the first evidence of DA production by Pseudo-nitzschia species stimulated in the presence of filter-feeding bivalves. The results of this study highlight complex interactions that can influence toxin production by Pseudo-nitzschia and accumulation in bivalves. These results will help to better understand the biotic factors that drive DA production by Pseudo-nitzschia and bivalve contamination during Pseudo-nitzschia blooms.

Acclimation of Isochrysis galbana Parke (Isochrysidaceae) for enhancing its tolerance and biodegradation to high-level phenol in seawater.

Marine microalgae with high removal efficiency of phenol are needed for the remediation of polluted seawater in cases involving phenol spills. To achieve this purpose, adaptive laboratory evolution (ALE) was performed by a microalga Isochrysis galbana Parke MACC/H59, which is capable of degrading phenol at concentrations of less than 100 mg L-1 in 4 d. Two acclimation conditions were used: (i) 90 d at 100 mg L-1 phenol, and (ii) 90 d at 100 mg L-1 phenol followed by another 90 d at 200 mg L-1 phenol. By doing so, two strains (PAS-1 and PAS-2) could be obtained respectively. They grew rapidly at phenol concentrations up to 200 mg L-1 and 300 mg L-1, respectively, with a specific growth rate 2.52-3.40 times and 1.93-3.23 times that of the control (without phenol). Also, both strains had a higher removal capacity of phenol than the unacclimated alga. Phenol at an initial concentration of 200 mg L-1 was completely removed in 5 d thereby. For 300 mg L-1 phenol, a removal efficiency of 92% was achieved in 10 days by using PAS-2, with a removal rate constant of 30.01 d-1 (about twice that of PAS-1) and a half-life of 4.90 d (about half that of PAS-1), showing that a better strain may be obtained by extending the acclimation time. The enhancement of phenol biodegradation can be explained by the elevated activity of phenol hydroxylase (PH) in both strains. These results indicated that ALE could be an efficient tool used to enhance the tolerance and biodegradation of marine microalgae to phenol in seawater.

Temperate infection in a virus-host system previously known for virulent dynamics.

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities.

Effects of florfenicol on growth, photosynthesis and antioxidant system of the non-target organism Isochrysis galbana.

Florfenicol (FFC) is one of the most universally used antibiotics in aquaculture, which is substitute for chloramphenicol extensively, while the massive residues in aquatic environment were assumed to threaten the non-target organisms. Present research investigated the effects of florfenicol on growth, chlorophyll content, photosynthesis, and antioxidant ability of Isochrysis galbana. The results showed that FFC at 0.001-1 mg/L stimulated the growth of I. galbana and increased the content of chlorophyll. In addition, photosynthesis of I. galbana was inhibited and the photosynthetic parameters were uplifted with the increased exposure duration and FFC concentration. Furthermore, superoxide dismutase (SOD), catalase (CAT) activity significantly dropped at 0.01-20 mg/L FFC, while the contents of malondialdehyde (MDA), glutathione (GSH) and reactive oxygen species (ROS) increased after 72 h exposure, indicating that FFC at high concentrations caused a serious oxidative stress on algae. The simultaneous increase of ROS disrupted the equilibration between oxidants and antioxidant systems. Under the high concentration of FFC, the excessive of ROS was generated in algae which affected the membrane permeability and further decreased the cell biomass. Present study showed that acute exposure (72 h) at the environmental relevant concentration (0.01 mg/L) cannot induce the physiological dysfunction of the microalgae I. galbana, but the feeding concentration (20 mg/L) can. Additionally, this study hinted the possible negative impacts on ecosystems with the chronic exposure even at low FFC concentration or with the uncontrolled use of FFC.

Coccolith mass and morphology of different Emiliania huxleyi morphotypes: A critical examination using Canary Islands material.

Different morphotypes of the abundant marine calcifying algal species Emiliania huxleyi are commonly linked to various degrees of E. huxleyi calcification, but few studies have been done to validate this assumption. This study investigated therefore whether E. huxleyi morphotypes can be related to coccolithophore calcification and coccolith mass. Samples from January (high productivity) and September (low productivity) 1997 at an open ocean and a coastal site near the Canary Islands were analysed using a combination of thickness measurements (Circular Polarizer Retardation estimates (CPR) method), Scanning Electron Microscope imaging, and Markov Chain Monte Carlo (MCMC) models. Mean E. huxleyi coccolith mass varied from a maximum of 2.9pg at the open ocean station in January to a minimum of 1.7pg in September at both stations. In contrast, overall calcite produced by E. huxleyi (assuming 23 coccoliths/cell) varied from a maximum of 2.6 µgL-1 at the coastal station in January to a minimum of 0.5 µgL-1 in September at the open ocean site. The relative abundance of "Overcalcified" Type A, Type A, Group B and malformed coccoliths was determined from SEM images. The mean coccolith mass of "Overcalcified" Type A was 2.0pg using the CPR-method, while mean mass of Type A and Group B coccoliths was determined using coccolith length measurements from SEM images and MCMC models relating thickness measurements to morphotype relative abundance. Type A cocccolith mass varied from a 1.6pg to 2.6pg and Group B coccolith mass varied from 1.5pg to 2.0pg. These results demonstrate that the coccolith mass of Type A, "Overcalcified" Type A, and Group B do not differ systematically and there is no systematic relationship between relative abundance of a morphotype and the overall calcite production of E. huxleyi. Therefore, morphotype appearance and relative abundance can not be uniformly used as reliable indicators of E. huxleyi calcification or calcite production.

Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators.

Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica, a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption.

De novo transcriptome profile of coccolithophorid alga Emiliania huxleyi CCMP371 at different calcium concentrations with proteome analysis.

The haptophyte alga Emiliania huxleyi is the most abundant coccolithophore in the modern ocean and produces elaborate calcite crystals, called coccolith, in a separate intracellular compartment known as the coccolith vesicle. Despite the importance of biomineralization in coccolithophores, the molecular mechanism underlying it remains unclear. Understanding this precise machinery at the molecular level will provide the knowledge needed to enable further manipulation of biomineralization. In our previous study, altering the calcium concentration modified the calcifying ability of E. huxleyi CCMP371. Therefore in this study, we tested E. huxleyi cells acclimated to three different calcium concentrations (0, 0.1, and 10 mM). To understand the whole transcript profile at different calcium concentrations, RNA-sequencing was performed and used for de novo assembly and annotation. The differentially expressed genes (DEGs) among the three different calcium concentrations were analyzed. The functional classification by gene ontology (GO) revealed that 'intrinsic component of membrane' was the most enriched of the GO terms at the ambient calcium concentration (10 mM) compared with the limited calcium concentrations (0 and 0.1 mM). Moreover, the DEGs in those comparisons were enriched mainly in 'secondary metabolites biosynthesis, transport and catabolism' and 'signal transduction mechanisms' in the KOG clusters and 'processing in endoplasmic reticulum', and 'ABC transporters' in the KEGG pathways. Furthermore, metabolic pathways involved in protein synthesis were enriched among the differentially expressed proteins. The results of this study provide a molecular profile for understanding the expression of transcripts and proteins in E. huxleyi at different calcium concentrations, which will help to identify the detailed mechanism of its calcification.

Physiological responses of a coccolithophore to multiple environmental drivers.

Ocean acidification is known to affect primary producers differentially in terms of species and environmental conditions, with controversial results obtained under different experimental setups. In this work we examined the physiological performances of the coccolithophore Gephyrocapsa oceanica that had been acclimated to 1000 µatm CO2 for ~400 generations, and then exposed to multiple drivers, light intensity, light fluctuating frequency, temperature and UV radiation. Here, we show that increasing light intensity resulted in higher non-photochemical quenching and the effective absorption cross-section of PSII. The effective photochemical efficiency (Fv'/Fm') decreased with increased levels of light, which was counterbalanced by fluctuating light regimes. The greenhouse condition acts synergistically with decreasing fluctuating light frequency to increase the Fv'/Fm' and photosynthetic carbon fixation rate. Our data suggest that the coccolithophorid would be more stressed with increased exposures to solar UV irradiances, though its photosynthetic carbon fixation could be enhanced under the greenhouse condition.

Relationship between coccolith length and thickness in the coccolithophore species Emiliania huxleyi and Gephyrocapsa oceanica.

Coccolith mass is an important parameter for estimating coccolithophore contribution to carbonate sedimentation, organic carbon ballasting and coccolithophore calcification. Single coccolith mass is often estimated based on the ks model, which assumes that length and thickness increase proportionally. To evaluate this assumption, this study compared coccolith length, thickness, and mass of seven Emiliania huxleyi strains and one Gephyrocapsa oceanica strain grown in 25, 34, and 44 salinity artificial seawater. While coccolith length increased with salinity in four E. huxleyi strains, thickness did not increase significantly with salinity in three of these strains. Only G. oceanica showed a consistent increase in length with salinity that was accompanied by an increase in thickness. Coccolith length and thickness was also not correlated in 14 of 24 individual experiments, and in the experiments in which there was a positive relationship r2 was low (<0.4). Because thickness did not increase with length in E. huxleyi, the increase in mass was less than expected from the ks model, and thus, mass can not be accurately estimated from coccolith length alone.

Growth Inhibition of Phaeocystis Globosa Induced by Luteolin-7-O-glucuronide from Seagrass Enhalus acoroides.

Enhalus acoroides (E. acoroides) is one of the most common species in seagrass meadows. Based on the application of allelochemicals from aquatic plants to inhibit harmful algal blooms (HABs), we used E. acoroides aqueous extract against harmful algae species Phaeocystis globosa (P. globosa). The results showed that E. acoroides aqueous extract could significantly inhibited the growth of P. globosa, decrease the chlorophyll-a content and photosynthetic efficiency (Fv/Fm) values of P. globosa, followed by vacuolization, plasmolysis, and the destruction of organelles. Twelve types of major chemical constituents were identified in E. acoroides aqueous extracts by ultraperformance liquid chromatography-high resolution mass spectrometry (UPLC-HRMS), including six flavonoids, two homocyclic peptides, two long-chain aliphatic amides, one tannin, and one nitrogen heterocyclic compound. Flavonoids were the characteristic chemical constituents of E. acoroides aqueous extract. Furthermore, the antialgal activity of luteolin-7-O-glucuronide (68.125 µg/mL in 8 g/L E. acoroides aqueous extract) was assessed. The EC50-96 h value was 34.29 µg/mL. In conclusion, the results revealed that luteolin 7-O-glucuronide was one of the antialgal compounds of E. acoroides aqueous extract, with potential application as novel algaecide.

Prymnesium parvum differentially triggers sublethal fish antioxidant responses in vitro among salinity and nutrient conditions.

Significant fish kills have been attributed to Prymnesium parvum in coastal and inland waters around the world. However, specific mechanisms responsible for adverse outcomes resulting from this harmful algal bloom (HAB) species remain unclear, though the gill has previously been identified as an important target organ. In the present study, an in vitro approach was used to examine cytotoxicity and antioxidant responses in fish liver (Hepa-E1 and PLHC-1) and gill (G1B and RTgill-W1) cell lines, following exposure to P. parvum grown at different salinities and nutrient concentrations, which can influence the magnitude of acute toxicity. Cultures from high salinity compromised survival of hepatic cell lines exposed to high dilutions, whereas no significant cytotoxicity was observed for gill cell lines. With respect to control groups, catalase showed significant activity in both gill cell lines, especially RTgill-W1, following exposure to high salinity cultures. High levels of superoxide dismutase were measured in Hepa-E1 cells exposed to all experimental treatment combinations and in RTgill-W1 cells following exposure to high salinity conditions, with respect to non-exposed cells Glutathione peroxidase activity was also detected at significant levels in Hepa-E1 cells after exposure to cultures from high salinity and the low salinity X low nutrients. Slight GPx increases were only observed in PLHC-1 and G1B exposed to P. parvum grown at high salinity. These results suggest that: 1. specific combinations of salinity and nutrient levels may contribute to production and potency of P. parvum toxins resulting in sub-lethal effects, and 2. sub-lethal responses are more prominent than cytotoxicity, and that oxidative stress may be a significant adverse effect of toxins produced by P. parvum.

Toxicity of binary mixtures of pesticides to the marine microalgae Tisochrysis lutea and Skeletonema marinoi: Substance interactions and physiological impacts.

This study screened binary mixtures of pesticides for potential synergistic interaction effects on growth of the marine microalgae Tisochrysis lutea and Skeletonema marinoi. It also examined the single and combined effects of three of the most toxic substances on microalgal physiology. Single substances were first tested on each microalgal species to determine their respective EC50 and concentration-response relationships. The toxicity of six and seven binary mixtures was then evaluated in microplate experiments on the growth of T. lutea and S. marinoi, respectively, using two mixture modelling approaches: isobolograms and the MIXTOX tool, based on Concentration Addition (CA) or Independent Action (IA) models. Significant cases of antagonism (for both species) and synergism (for S. marinoi) were observed for the mixtures of isoproturon and spiroxamine, and isoproturon and metazachlor, respectively. These two mixtures, together with that of isoproturon and diuron, for which additivity was observed, were further studied for their impacts on the physiology of each species. Exposures were thus made in culture flasks at three concentrations, or concentration combinations for mixtures, selected to cause 25%, 50% and 75% growth rate inhibition. The effects of the selected pesticides singly and in combination were evaluated at three perceived effect concentrations on esterase metabolic activity, relative lipid content, cytoplasmic membrane potential and reactive oxygen species (ROS) content by flow cytometry, and on photosynthetic quantum yield (ϕ'M) by PAM-fluorescence. Isoproturon and diuron singly and in mixtures induced 20-40% decreases in ϕ'M which was in turn responsible for a significant decrease in relative lipid content for both species. Spiroxamine and metazachlor were individually responsible for an increase in relative lipid content (up to nearly 300% for metazachlor on S. marinoi), as well as cell depolarization and increased ROS content. The mixture of isoproturon and metazachlor tested on S. marinoi caused a 28-34% decrease in ϕ'M that was significantly higher than levels induced by each of substances when tested alone. This strong decrease in ϕ'M could be due to a combined effect of these substances on the photosynthetic apparatus, which is likely the cause of the synergy found for this mixture.

Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis.

Photosymbiosis between single-celled hosts and microalgae is common in oceanic plankton, especially in oligotrophic surface waters. However, the functioning of this ecologically important cell-cell interaction and the subcellular mechanisms allowing the host to accommodate and benefit from its microalgae remain enigmatic. Here, using a combination of quantitative single-cell structural and chemical imaging techniques (FIB-SEM, nanoSIMS, Synchrotron X-ray fluorescence), we show that the structural organization, physiology, and trophic status of the algal symbionts (the haptophyte Phaeocystis) significantly change within their acantharian hosts compared to their free-living phase in culture. In symbiosis, algal cell division is blocked, photosynthesis is enhanced, and cell volume is increased by up to 10-fold with a higher number of plastids (from 2 to up to 30) and thylakoid membranes. The multiplication of plastids can lead to a 38-fold increase of the total plastid volume in a cell. Subcellular mapping of nutrients (nitrogen and phosphorous) and their stoichiometric ratios shows that symbiotic algae are impoverished in phosphorous and suggests a higher investment in energy-acquisition machinery rather than in growth. Nanoscale imaging also showed that the host supplies a substantial amount of trace metals (e.g., iron and cobalt), which are stored in algal vacuoles at high concentrations (up to 660 ppm). Sulfur mapping reveals a high concentration in algal vacuoles that may be a source of antioxidant molecules. Overall, this study unveils an unprecedented morphological and metabolic transformation of microalgae following their integration into a host, and it suggests that this widespread symbiosis is a farming strategy wherein the host engulfs and exploits microalgae.