Uneven response of phytoplankton-bacteria coupling under Saharan dust pulse and ultraviolet radiation in the south-western Mediterranean Sea.

The microbial carbon (C) flux in the ocean is a key functional process governed by the excretion of organic carbon by phytoplankton (EOC) and heterotrophic bacterial carbon demand (BCD). Ultraviolet radiation (UVR) levels in upper mixed layers and increasing atmospheric dust deposition from arid regions may alter the degree of coupling in the phytoplankton-bacteria relationship (measured as BCD:EOC ratio) with consequences for the C-flux through these compartments in marine oligotrophic ecosystem. Firstly, we performed a field study across the south-western (SW) Mediterranean Sea to assess the degree of coupling (BCD:EOC) and how it may be related to metabolic balance (total primary production: community respiration; PPT:CR). Secondly, we conducted a microcosm experiment in two contrasting areas (heterotrophic nearshore and autotrophic open sea) to test the impact of UVR and dust interaction on microbial C flux. In the field study, we found that BCD was not satisfied by EOC (i.e., BCD:EOC >1; uncoupled phytoplankton-bacteria relationship). BCD:EOC ratio was negatively related to PPT:CR ratio across the SW Mediterranean Sea. A spatial pattern emerged, i.e. in autotrophic open sea stations uncoupling was less severe (BCD:EOC ranged 1-2), whereas heterotrophic nearshore stations uncoupling was more severe (BCD:EOC > 2). In the experimental study, in the seawater both enriched with dust and under UVR, BCD:EOC ratio decreased by stimulating autotrophic processes (particulate primary production (PPP) and EOC) in the heterotrophic nearshore area, whereas BCD:EOC increased by stimulating heterotrophic processes [heterotrophic bacterial production (HBP), bacterial growth efficiency (BGE), bacterial respiration (BR)] in the autotrophic open sea. Our results show that this spatial pattern could be reversed under future UVR × Dust scenario. Overall, the impact of greater dust deposition and higher UVR levels will alter the phytoplankton-bacteria C-flux with consequences for the productivity of both communities, their standing stocks, and ultimately, the ecosystem's metabolic balance at the sea surface.

Dust storms increase the tolerance of phytoplankton to thermal and pH changes.

Aquatic communities are increasingly subjected to multiple stressors through global change, including warming, pH shifts, and elevated nutrient concentrations. These stressors often surpass species tolerance range, leading to unpredictable consequences for aquatic communities and ecosystem functioning. Phytoplankton, as the foundation of the aquatic food web, play a crucial role in controlling water quality and the transfer of nutrients and energy to higher trophic levels. Despite the significance in understanding the effect of multiple stressors, further research is required to explore the combined impact of multiple stressors on phytoplankton. In this study, we used a combination of crossed experiment and mechanistic model to analyze the ecological and biogeochemical effects of global change on aquatic ecosystems and to forecast phytoplankton dynamics. We examined the effect of dust (0-75 mg L-1 ), temperature (19-27°C), and pH (6.3-7.3) on the growth rate of the algal species Scenedesmus obliquus. Furthermore, we carried out a geospatial analysis to identify regions of the planet where aquatic systems could be most affected by atmospheric dust deposition. Our mechanistic model and our empirical data show that dust exerts a positive effect on phytoplankton growth rate, broadening its thermal and pH tolerance range. Finally, our geospatial analysis identifies several high-risk areas including the highlands of the Tibetan Plateau, western United States, South America, central and southern Africa, central Australia as well as the Mediterranean region where dust-induced changes are expected to have the greatest impacts. Overall, our study shows that increasing dust storms associated with a more arid climate and land degradation can reverse the negative effects of high temperatures and low pH on phytoplankton growth, affecting the biogeochemistry of aquatic ecosystems and their role in the cycles of the elements and tolerance to global change.

Fluctuation at High Temperature Combined with Nutrients Alters the Thermal Dependence of Phytoplankton.

The Metabolic Theory of Ecology (MTE) predicts that the temperature increases exert a common effect on organisms stimulating metabolic rates, this being stronger for a heterotrophic than for an autotrophic metabolism. However, no available studies within the MTE framework have focused on organisms' response under fluctuation at high temperature interacting with factors such as nutrient availability, or how this interaction could affect the coexistence between mixotrophic and strict autotrophic phytoplankton. Hence, we assess how the phytoplankton metabolism and species composition are affected under scenarios of high temperature and fluctuation at high temperature, and how nutrients alter the direction and magnitude of such impact. For that, we use a mixed culture composed of two phytoplankton species: a strict autotrophic species and a mixotrophic species. Our results indicate that, in agreement with the MTE, only fluctuation at high temperature treatment registered a greater activation energy (Ea) value for respiration than for primary production and stimulated mixotrophic over strict autotrophic species abundance compared to control treatment. Remarkably, fluctuation at high temperature had a strong negative impact on the total abundance of the mixed-culture. The interaction between nutrient enrichment and fluctuation at high temperature increased abundance of the strict autotrophic species and overall species abundance, and led to Ea values that were higher in primary production than in respiration. Changes in community composition, enhanced by nutrient enrichment, could be behind this response, which can have implications in ecosystem functioning in a changing world.

Microbial plankton responses to multiple environmental drivers in marine ecosystems with different phosphorus limitation degrees.

Multiple drivers are threatening the functioning of the microbial food webs and trophic interactions. Our understanding about how temperature, CO2, nutrient inputs, and solar ultraviolet radiation (UVR) availability interact to alter ecosystem functioning is scarce because research has focused on single and double interactions. Moreover, the role that the degree of in situ nutrient limitation could play in the outcome of these interactions has been largely neglected, despite it is predominant in marine ecosystems. We address these uncertainties by combining remote-sensing analyses, and a collapsed experimental design with natural microbial communities from Mediterranean Sea and Atlantic Ocean exposed to temperature, nutrients, CO2, and UVR interactions. At the decade scale, we found that more intense and frequent (and longer lasting) Saharan dust inputs (and marine heatwaves) were only coupled with reduced phytoplankton biomass production. When microbial communities were concurrently exposed to future temperature, CO2, nutrient, and UVR conditions (i.e. the drivers studied over long-term scales), we found shifts from net autotrophy [primary production:respiration (PP:R) ratio > 1] towards a metabolic equilibrium (PP:R ratio ~ 1) or even a net heterotrophy (PP:R ratio < 1), as P-limitation degree was higher (i.e. Atlantic Ocean). These changes in the metabolic balance were coupled with a weakened phytoplankton-bacteria interaction (i.e. bacterial carbon demand exceeded phytoplankton carbon supply. Our work reveals that an accentuated in situ P limitation may promote reductions both in carbon uptake and fluxes between trophic levels in microbial plankton communities under global-change conditions. We show that considering long-term series can aid in identifying major local environmental drivers (i.e. temperature and nutrients in our case), easing the design of future global-change studies, but also that the abiotic environment to which microbial plankton communities are acclimated should be taken into account to avoid biased predictions concerning the effects of multiple interacting global-change drivers on marine ecosystems.

Housekeeping in the Hydrosphere: Microbial Cooking, Cleaning, and Control under Stress.

Who's cooking, who's cleaning, and who's got the remote control within the waters blanketing Earth? Anatomically tiny, numerically dominant microbes are the crucial "homemakers" of the watery household. Phytoplankton's culinary abilities enable them to create food by absorbing sunlight to fix carbon and release oxygen, making microbial autotrophs top-chefs in the aquatic kitchen. However, they are not the only bioengineers that balance this complex household. Ubiquitous heterotrophic microbes including prokaryotic bacteria and archaea (both "bacteria" henceforth), eukaryotic protists, and viruses, recycle organic matter and make inorganic nutrients available to primary producers. Grazing protists compete with viruses for bacterial biomass, whereas mixotrophic protists produce new organic matter as well as consume microbial biomass. When viruses press remote-control buttons, by modifying host genomes or lysing them, the outcome can reverberate throughout the microbial community and beyond. Despite recognition of the vital role of microbes in biosphere housekeeping, impacts of anthropogenic stressors and climate change on their biodiversity, evolution, and ecological function remain poorly understood. How trillions of the smallest organisms in Earth's largest ecosystem respond will be hugely consequential. By making the study of ecology personal, the "housekeeping" perspective can provide better insights into changing ecosystem structure and function at all scales.

Regulation of Phagotrophy by Prey, Low Nutrients, and Low Light in the Mixotrophic Haptophyte Isochrysis galbana.

Mixotrophy combines autotrophy and phagotrophy in the same cell. However, it is not known to what extent the phagotrophy influences metabolism, cell composition, and growth. In this work, we assess, on the one hand (first test), the role of phagotrophy on the elemental and biochemical composition, cell metabolism, and enzymes related to C, N, and S metabolism of Isochrysis galbana Parke, 1949. On the other hand, we study how a predicted increase of phagotrophy under environmental conditions of low nutrients (second test) and low light (third test) can affect its metabolism and growth. Our results for the first test revealed that bacterivory increased the phosphorous and iron content per cell, accelerating cell division and improving the cell fitness; in addition, the stimulation of some C and N enzymatic routes help to maintain, to some degree, compositional homeostasis. Under nutrient or light scarcity, I. galbana grew more slowly despite greater bacterial consumption, and the activities of key enzymes involved in C, N, and S metabolism changed according to a predominantly phototrophic strategy of nutrition in this alga. Contrary to recent studies, the stimulation of phagotrophy under low nutrient and low irradiance did not imply greater and more efficient C flux.

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment.

Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions.IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.

Mixotrophic trade-off under warming and UVR in a marine and a freshwater alga.

Mixotrophic protists combine phagotrophy and phototrophy within a single cell. Greater phagotrophic activity could reinforce the bypass of carbon (C) flux through the bacteria-mixotroph link and thus lead to a more efficient transfer of C and other nutrients to the top of the trophic web. Determining how foreseeable changes in temperature and UVR affect mixotrophic trade-offs in favor of one or the other nutritional strategy, along the mixotrophic gradient, is key to understanding the fate of carbon and mineral nutrients in the aquatic ecosystem. Our two main hypotheses were: (i) that increased warming and UVR will divert metabolism toward phagotrophy, and (ii) that the magnitude of this shift will vary according to the organism's position along the mixotrophic gradient. To test these hypotheses, we used two protists (Isochrysis galbana and Chromulina sp.) located in different positions on the mixotrophic gradient, subjecting them to the action of temperature and of UVR and their interaction. Our results showed that the joint action of these two factors increased the primary production:bacterivory ratio and stoichiometric values (N:P ratio) close to Redfield's ratio. Therefore, temperature and UVR shifted the metabolism of both organisms toward greater phototrophy regardless of the original position of the organism on the mixotrophic gradient. Weaker phagotrophic activity could cause a less efficient transfer of C to the top of trophic webs.

A shifting balance: responses of mixotrophic marine algae to cooling and warming under UVR.

Mixotrophy is a dominant metabolic strategy in ecosystems worldwide. Shifts in temperature (T) and light (i.e. the ultraviolet portion of spectrum (UVR)) are key abiotic factors that modulate the conditions under which an organism is able to live. However, whether the interaction between both drivers alters mixotrophy in a global-change context remains unassessed. To determine the T × UVR effects on relative electron transport rates, nonphotochemical quenching, bacterivory, and bacterial production, we conducted an experiment with Isochrysis galbana populations grown mixotrophically, which were exposed to 5°C of cooling and warming with respect to the control (19°C) with (or without) UVR over light-dark cycles and different timescales. At the beginning of the experiment, cooling inhibited the relative electron transport and bacterivory rates, whereas warming depressed only bacterivory regardless of the radiation treatment. By the end of the experiment, warming and UVR conditions stimulated bacterivory. These reduced relative electron transport rates (c. 50% (warming) and > 70% (cooling)) were offset by increased (35%) cumulative bacterivory rates under warming and UVR conditions. We propose that mixotrophy constitutes an energy-saving and a compensatory mechanism to gain carbon (C) when photosynthesis is impaired, and highlight the need to consider the natural environmental changes affecting the populations when we test the impacts of interacting global-change drivers.

Climate-driven shifts in algal-bacterial interaction of high-mountain lakes in two years spanning a decade.

Algal-bacterial interactions include mutualism, commensalism, and predation. However, how multiple environmental conditions that regulate the strength and prevalence of a given interaction remains unclear. Here, we test the hypothesis that the prevailing algal-bacterial interaction shifted in two years (2005 versus 2015), due to increased temperature (T) and Saharan dust depositions in high-mountain lakes of Sierra Nevada (S Spain). Our results support the starting hypothesis that the nature of the prevailing algal-bacterial interaction shifted from a bacterivory control exerted by algae to commensalism, coinciding with a higher air and water T as well as the lower ratio sestonic nitrogen (N): phosphorous (P), related to greater aerosol inputs. Projected global change conditions in Mediterranean region could decline the functional diversity and alter the role of mixotrophy as a carbon (C) by-pass in the microbial food web, reducing the biomass-transfer efficiency up the web by increasing the number of trophic links.

Growth impacts of Saharan dust, mineral nutrients, and CO2 on a planktonic herbivore in southern Mediterranean lakes.

Rising levels of CO2 can boost plant biomass but reduce its quality as a food source for herbivores. However, significant uncertainties remain as to the degree to which the effect is modulated by other environmental factors and the underlying processes causing these responses in nature. To address these questions, we carried out CO2-manipulation experiments using natural seston from three lakes under nutrient-enriched conditions (mimicking eutrophication and atmospheric dust-input processes) as a food source for the planktonic Daphnia pulicaria. Contrary to expectations, there were no single effects of rising CO2 on herbivorous growth. Instead, synergistic CO2 × nutrient interactions indicated that CO2 did not support higher zooplankton growth rates unless supplemented with dust or inorganic nutrients (nitrogen, N; phosphorus, P) in two of three studied lakes. The overall positive correlation between zooplankton growth and seston carbon (C), but not seston C:P, suggested that this was a food quantity-mediated response. In addition, we found that this correlation improved when the data were grouped according to the nutrient treatments, and that the response was largest for dust. The synergistic CO2 × nutrient effects reported here imply that the effects of rising CO2 levels on herbivorous growth may be strongly influenced by eutrophication processes and the increase in dust deposition predicted for the Mediterranean region.

Saharan dust inputs and high UVR levels jointly alter the metabolic balance of marine oligotrophic ecosystems.

The metabolic balance of the most extensive bioma on the Earth is a controversial topic of the global-change research. High ultraviolet radiation (UVR) levels by the shoaling of upper mixed layers and increasing atmospheric dust deposition from arid regions may unpredictably alter the metabolic state of marine oligotrophic ecosystems. We performed an observational study across the south-western (SW) Mediterranean Sea to assess the planktonic metabolic balance and a microcosm experiment in two contrasting areas, heterotrophic nearshore and autotrophic open sea, to test whether a combined UVR × dust impact could alter their metabolic balance at mid-term scales. We show that the metabolic state of oligotrophic areas geographically varies and that the joint impact of UVR and dust inputs prompted a strong change towards autotrophic metabolism. We propose that this metabolic response could be accentuated with the global change as remote-sensing evidence shows increasing intensities, frequencies and number of dust events together with variations in the surface UVR fluxes on SW Mediterranean Sea. Overall, these findings suggest that the enhancement of the net carbon budget under a combined UVR and dust inputs impact could contribute to boost the biological pump, reinforcing the role of the oligotrophic marine ecosystems as CO2 sinks.