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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.

We thank R/V UCÁDIZ crew, and Eulogio Corral by their help during seawater sampling. Cristina Estevan-Pardo is acknowledged by her collaboration during the experiments, and David Nesbitt for the English proofreading. Comments and suggestions by the Associated Editor Dr. Blasco and three anonymous reviewers are deeply acknowledged. This research was funded by ‘convocatoria de proyectos de jóvenes investigadores CEIMAR 2018’ from Campus de Excelencia Internacional del Mar (MIXOCOST, CEIJ-008 to MJC), and by Ministerio de Economía y Competitividad and Fondo Europeo de Desarrollo regional (FEDER) (METAS, CGL2015-67682-R to PC and JMM-S). MJC was supported by Juan de la Cierva-Formación ( FJCI2017-32318 ) and Incorporación ( IJC2019-040850-I ) grants from Ministerio de Ciencia, Innovación y Universidades . JMG-O was supported by University of Granada through programa de promoción y empleo joven from Junta de Andalucía and FEDER ( PEJ2018-003106-A ), and DS-G by METAS project., 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., Campus de Excelencia Internacional del Mar, Fondo Europeo de Desarrollo, Incorporación IJC2019-040850-I, METAS, MIXOCOST CEIJ-008, Ministerio de Ciencia, Innovación y Universidades, Ministerio de Economía y Competitividad, Universidad de Granada, European Regional Development Fund CGL2015-67682-R, FJCI2017-32318, Junta de Andalucía PEJ2018-003106-A

[EN] Freshwater ecosystems are exposed to an increasing number of stressors, challenging their biomonitoring and management. Despite recent advances in multiple-stressor research, regional-scale assessments in areas with high freshwater biodiversity and increasing anthropogenic pressure are urgently needed. We reviewed 61 studies focused on freshwater individuals, populations and communities from the Iberian Peninsula to (i) quantify the frequency of experimental approaches used (manipulative, observational), aquatic systems, biological organization levels, and types of organisms and modelled responses, (ii) identify key individual stressors and the frequency of significant positive (increase in response magnitude) and negative (decrease) effects and (iii) determine types of interacting stressors and the frequency of their combined effects. Our dataset comprised 409 unique responses to 13 types of individual stressors, 34 stressor pairs and 12 high-order interactions (3- and 4-way). We found a higher prevalence of manipulative (85 %) respect to observational studies, and a greater focus on lotic systems (59 %) and heterotrophic organisms (58 %). The most studied stressors were nutrient (Nutr), thermal (Therm), hydrologic (Hydr), ultraviolet radiation (UVR), toxic (Toxic) and salinity (Sal) stress and land-use pressure. Individual stressors showed a higher proportion of negative (34 %) than positive effects (26 %). Nutr × UVR, Toxic × Toxic, Therm × Toxic, Hydr × Toxic, Sal × Therm, and Nutr × Therm were the most studied stressor pairs. Non-interactive (50 %) and interactive responses (50 %) were balanced. Antagonistic effects (18 %) were slightly more common than synergisms (15 %), reversal or opposing. (13 %) and high-order interactions (4 %). Such proportions varied within experimental approaches, biological organization levels and organism types. Our findings are helpful to manage certain stressor combinations in Iberian freshwaters. Further efforts in Iberian multiple-stressor research should be directed to (i) intensify the study of lentic systems, (ii) explore more observational data, (iii) autotrophic organisms and (vi) biodiversity-ecosystem functioning responses, and (v) cover a wider range of stressors and (vi) more complex interacting stressor scenarios., [ES] Los ecosistemas acuáticos continentales están expuestos a un creciente número de factores de estrés, lo que supone un reto para su monitoreo y gestión. A pesar de los recientes avances en el estudio de estresores múltiples a nivel global, resulta también necesario evaluar áreas que concentran una alta biodiversidad acuática y que están expuestas a una elevada presión antrópica. En esta revisión hemos examinado 61 estudios basados en individuos, poblaciones y comunidades de ecosistemas acuáticos continentales ibéricos para (i) cuantificar la frecuencia de la aproximación experimental usada (estudio manipulativo u observacional), el tipo de sistema acuático, niveles de organización biológica, tipos de organismos y de respuestas abarcadas, (ii) identificar estresores clave y la frecuencia de efectos positivos (aumento de magnitud de la respuesta) y negativos (descenso) y (iii) determinar las combinaciones de factores estudiados y la frecuencia de sus efectos combinados. Los estudios revisados incluyen 409 respuestas, 13 estresores individuales, 34 pares de estresores y 12 interacciones de orden superior (3er y 4º orden). Encontramos una mayor frecuencia de estudios manipulativos (85 %), en sistemas lóticos (59 %) y con organismos heterótrofos (58 %). Los estresores más estudiados fueron los nutrientes (Nutr), la temperatura (Therm), la hidrología (Hydr), la radiación ultravioleta (UVR), los tóxicos (Toxic), la salinidad (Sal) y cambios en los usos del suelo. Los efectos individuales fueron más frecuentemente negativos (34 %) que positivos (26 %). Los efectos combinados no interactivos (50 %) e interactivos (50 %) tuvieron una frecuencia similar. Los antagonismos (18 %) fueron ligeramente más frecuentes que los sinergismos (15 %), efectos reversos u opuestos (13 %) y las interacciones de orden superior (4 %). Sin embargo, estas proporciones varían notablemente entre tipos de estudios, niveles de organización biológica y tipos de organismos. Nuestros resultados son útiles para predecir y gestionar los efectos de ciertas combinaciones de estresores en los ecosistemas acuáticos ibéricos. Las investigaciones futuras sobre estresores múltiples en el contexto Ibérico deberían: (i) intensificar el estudio de los sistemas lénticos, (ii) explorar más datos observacionales, (iii) organismos autótrofos y (iv) respuestas de la relación biodiversidad-funcionamiento del ecosistema y (v) cubrir un rango más amplio de factores estresantes y (vi) escenarios de estresores interactivos más complejos., We thank the Asociación Ibérica de Limnología for inviting us to contribute with this article and the editors and referees that kindly revised previous versions of this manuscript. CG-C was supported by a “Juan de la Cierva – Incorporación” contract from Ministerio de Ciencia e Innovación (MICINN, IJC2018-036642-I). RA-R held a pre-doctoral grant BES-2015-073961 (FPI) funded by Ministerio de Economía y Competitividad. DB was funded by “PTI ECOBIODIV” through the “Vicepresidencia Adjunta de Áreas Científico-Técnicas (VAACT-CSIC). MJC was support ed by Juan de la Cierva-Formación (FJCI-2017-32318) and Incorporación (IJC2019-040850-I) contracts from MICINN. JMG-O was funded by University of Granada through Programa de Promoción y Empleo joven from Junta de Andalucía and FEDER (PEJ2018-003106-A). FP was funded by “Consejería de Economía, Conocimiento, Empresas y Universidad de la Junta de Andalucía-Fondo Social Europeo de Andalucía 2014-2020”. DS-F was supported by a Ramón y Cajal contract (RYC2019-027446-I), and SP by a “Juan de la Cierva-Formación” postdoctoral contract MICINN, FJC2018-035577-I).

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., National Science Foundation (NSF) EAR1637093 OCE 2346958, National Aeronautics and Space Administration-Michigan Space Grant Consortium Graduate Fellowships NNX15AJ20H, Spanish Government FEDER-CGL2015-67682-R, Fondo Europeo de Desarrollo Regional Project FEDER-CGL2015-67682-R, Junta de Andalucía P12-RNM 327, Spanish Government Fellowship "Formacion de Profesorado Universitario" Grant FPU14/00977

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.

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., 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.

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.

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.

Eutrophication, global warming, and rising carbon dioxide (CO2) levels are the three most prevalent pressures impacting the biosphere. Despite their individual effects are well-known, it remains untested how oligotrophication (i.e. nutrients reduction) can alter the planktonic community responses to warming and elevated CO2 levels. Here, we performed an indoor mesocosm experiment to investigate the warming × CO2 interaction under a nutrient reduction scenario (40%) mediated by an in-lake management strategy (i.e. addition of a commercial solid-phase phosphorus sorbent -Phoslock®) on a natural freshwater plankton community. Biomass production increased under warming × CO2 relative to present-day conditions; however, a Phoslock®-mediated oligotrophication reduced such values by 30–70%. Conversely, the warming × CO2 × oligotrophication interaction stimulated the photosynthesis by 20% compared to ambient nutrient conditions, and matched with higher resource use efficiency (RUE) and nutrient demand. Surprisingly, at a group level, we found that the multi-stressors scenario increased the photosynthesis in eukaryotes by 25%, but greatly impaired in cyanobacteria (ca. −25%). This higher cyanobacterial sensitivity was coupled with a reduced light harvesting efficiency and compensation point. Since Phoslock®-induced oligotrophication unmasked a strong negative warming × CO2 effect on cyanobacteria, it becomes crucial to understand how the interplay between climate change and nutrient abatement actions may alter the, ecosystems functioning. With an integrative understanding of these processes, policy makers will design more appropriate management strategies to improve the ecological status of aquatic ecosystems without compromising their ecological attributes and functioning.

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.

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. Fil: Villar-Argaiz, Manuel. Universidad de Granada; España Fil: Cabrerizo, Marco J.. Universidad de Granada; España Fil: González-Olalla, Juan Manuel. Universidad de Granada; España Fil: Valiñas, Macarena Soledad. Fundación Playa Unión. Estación de Fotobiología Playa Unión; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Rajic, Sanja. Universidad de Granada; España Fil: Carrillo, Presentación. Universidad de Granada; España

Rising levels of CO

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., This work was funded by the Ministerio Español de Ciencia e Innovación (CGL2011–23681 and CGL2015-67682-R), and Campus de Excelencia Internacional del Mar (CeiMar). M.J.C. and J.M.G.-O. were supported by the Spanish Government Fellowship “Formación de Profesorado Universitario” (FPU12/01243 and FPU14/00977, respectively).