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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

Increases in rainfall, continental runoff, and atmospheric dust deposition are reducing water transparency in lakes worldwide (i.e. higher attenuation Kd). Also, ongoing alterations in multiple environmental drivers due to global change are unpredictably impacting phytoplankton responses and lakes functioning. Although both issues demand urgent research, it remains untested how the interplay between Kd and multiple interacting drivers affect primary productivity ( Pc). We manipulated four environmental drivers in an in situ experiment—quality of solar ultraviolet radiation (UVR), nutrient concentration (Nut), CO2 partial pressure ( CO2), and light regime (Mix)—to determine how the Pc of nine freshwater phytoplankton communities, found along a Kd gradient in Mediterranean ecosystems, changed as the number of interacting drivers increased. Our findings indicated that UVR was the dominant driver, its effect being between 3–60 times stronger, on average, than that of any other driver tested. Also, UVR had the largest difference in driver magnitude of all the treatments tested. A future UVR × CO2 × Mix × Nut scenario exerted a more inhibitory effect on Pc as the water column became darker. However, the magnitude of this synergistic effect was 40–60% lower than that exerted by double and triple interactions and by UVR acting independently. These results illustrate that although future global-change conditions could reduce Pc in Mediterranean lakes, multiple interacting drivers can temper the impact of a severely detrimental driver (i.e. UVR), particularly as the water column darkens. ; Ministerio de Economía y Competividad (MINECO) ; European Union (EU) MICROSENSCGL2011-23681 METAS-CGL2015-67682-R ; Medio Ambiente, Rural, y Marino PN2009/067 ; Junta de Andalucía CVI-02598 P09-RNM-5376 ; Fundación Playa Unión (Argentina) ; Juan de la Cierva-Formacion from the Ministerio de Ciencia, Innovación y Universidades FJCI2017-32318 ; Postdoctoral contract "Contrato Puente" from Plan Propio (FP7/2017) of the University of Granada ; METAS project

Solar radiation and nutrient pulses regulate the ecosystem's functioning. However, little is known about how a greater frequency of pulsed nutrients under high ultraviolet radiation (UVR) levels, as expected in the near future, could alter the responses and interaction between primary producers and decomposers. In this report, we demonstrate through a mesocosm study in lake La Caldera (Spain) that a repeated (press) compared to a one-time (pulse) schedule under UVR prompted higher increases in primary (PP) than in bacterial production (BP) coupled with a replacement of photoautotrophs by mixotrophic nanoflagellates (MNFs). The mechanism underlying these amplified phytoplanktonic responses was a dual control by MNFs on bacteria through the excretion of organic carbon and an increased top-down control by bacterivory. We also show across a 6-year whole-lake study that the changes from photoautotrophs to MNFs were related mainly to the frequency of pulsed nutrients (e.g. desert dust inputs). Our results underscore how an improved understanding of the interaction between chronic and stochastic environmental factors is critical for predicting ongoing changes in ecosystem functioning and its responses to climatically driven changes. ; This study was supported by the Ministerio de Economía y Competitividad and Fondo Europeo de Desarrollo Regional (FEDER) (CGL2011-23681 and CGL2015-67682-R to PC), Ministerio de Medio Ambiente, Rural, y Marino (PN2009/067 to PC) and Junta de Andalucía (Excelencia projects P09-RNM-5376 and P12-RNM-327 to PC and JMMS, respectively). M.J.C. was supported by the Spanish Government "Formación de Profesorado Universitario" PhD grant (FPU12/01243) and I.D.-G. by the Junta de Andalucía "Personal Investigador en Formación" PhD grant (FPI RNM-5376). This work is in partial fulfillment of the Ph. D. thesis of M.J.C.

Metabolic and stoichiometric theories of ecology have provided broad complementary principles to understand ecosystem processes across different levels of biological organization. We tested several of their cornerstone hypotheses by measuring the nucleic acid (NA) and phosphorus (P) content of crustacean zooplankton species in 22 high mountain lakes (Sierra Nevada and the Pyrenees mountains, Spain). The P-allocation hypothesis (PAH) proposes that the genome size is smaller in cladocerans than in copepods as a result of selection for fast growth towards P-allocation from DNA to RNA under P limitation. Consistent with the PAH, the RNA:DNA ratio was >8-fold higher in cladocerans than in copepods, although 'fast-growth' cladocerans did not always exhibit higher RNA and lower DNA contents in comparison to 'slow-growth' copepods. We also showed strong associations among growth rate, RNA, and total P content supporting the growth rate hypothesis, which predicts that fast-growing organisms have high P content because of the preferential allocation to P-rich ribosomal RNA. In addition, we found that ontogenetic variability in NA content of the copepod Mixodiaptomus laciniatus (intra- and interstage variability) was comparable to the interspecific variability across other zooplankton species. Further, according to the metabolic theory of ecology, temperature should enhance growth rate and hence RNA demands. RNA content in zooplankton was correlated with temperature, but the relationships were nutrient-dependent, with a positive correlation in nutrient-rich ecosystems and a negative one in those with scarce nutrients. Overall our results illustrate the mechanistic connections among organismal NA content, growth rate, nutrients and temperature, contributing to the conceptual unification of metabolic and stoichiometric theories. ; This research was supported by the Spanish Ministries of Science and Innovation (CGL2011-23681/BOS), and Environment, Rural and Marine Affairs (OAPN2009/067); 'Consejería de Innovación, Ciencia y Empresa – Junta de Andalucía' (Excelencia CVI-02598; P09-RNM-5376); The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and Stockholm University's strategic marine environmental research program 'Baltic Ecosystem Adaptive Management', and a Spanish government 'Formación de Profesorado Universitario' fellowship to F.J. Bullejos.

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).

An indirect effect of global warming is a reduction in the depth of the upper mixed layer (UML) causing organisms to be exposed to higher levels of ultraviolet (UVR, 280–400 nm) and photosynthetically active radiation (PAR, 400–700 nm). This can affect primary and bacterial production as well as the commensalistic phytoplankton–bacteria relationship. The combined effects of UVR and reduction in the depth of the UML were assessed on variables related to the metabolism of phytoplankton and bacteria, during in situ experiments performed with natural pico- and nanoplankton communities from two oligotrophic lakes with contrasting UVR transparency (high-UVR versus low-UVR waters) of southern Spain. The negative UVR effects on epilimnetic primary production (PP) and on heterotrophic bacterial production (HBP), intensified under increased stratification, were higher in the low-UVR than in the high-UVR lake, and stronger on the phytoplanktonic than on the heterotrophic bacterial communities. Under UVR and increased stratification, the commensalistic phytoplankton–bacteria relationship was strengthened in the high-UVR lake where excretion of organic carbon (EOC) rates exceeded the bacterial carbon demand (BCD; i.e., BCD : EOC(%) ratio 100). The greater UVR damage to phytoplankton and bacteria and the weakening of their commensalistic interaction found in the low-UVR lake indicates that these ecosystems would be especially vulnerable to UVR and increased stratification as stressors related to global climate change. Thus, our findings may have important implications for the carbon cycle in oligotrophic lakes of the Mediterranean region. ; This study was supported by the Ministerio Español de Medio Ambiente, Rural y Marino (PN2009/067), Ciencia e Innovación (CGL2011-23681), Junta de Andalucía (Excelencia CVI-02598 and P09-RNM-5376), Consejo Nacional de Investigaciones Científicas y Técnicas – CONICET (PIP no. 112-201001-00228), and Fundación Playa Unión. G. Herrera and C. Durán were supported by a Formación de Profesorado Universitario grant from the Spanish government. The authors are indebted to the staff of Sierra Nevada National Park and Lagunas de Ruidera Natural Park for permission to work, to E. Jiménez-Coll for the bacterial production analysis, and to D. Nesbitt for writing assistance in English.

The responses of heterotrophic microbial food webs (HMFW) to the joint action of abiotic stressors related to global change have been studied in an oligotrophic high-mountain lake. A 2×5 factorial design field experiment performed with large mesocosms for >2 months was used to quantify the dynamics of the entire HMFW (bacteria, heterotrophic nanoflagellates, ciliates, and viruses) after an experimental P-enrichment gradient which approximated or surpassed current atmospheric P pulses in the presence vs. absence of ultraviolet radiation. HMFW underwent a mid-term (<20 days) acute development following a noticeable unimodal response to P enrichment, which peaked at intermediate P-enrichment levels and, unexpectedly, was more accentuated under ultraviolet radiation. However, after depletion of dissolved inorganic P, the HMFW collapsed and was outcompeted by a low-diversity autotrophic compartment, which constrained the development of HMFW and caused a significant loss of functional biodiversity. The dynamics and relationships among variables, and the response patterns found, suggest the importance of biotic interactions (predation/parasitism and competition) in restricting HMFW development, in contrast to the role of abiotic factors as main drivers of autotrophic compartment. The response of HMFW may contribute to ecosystem resilience by favoring the maintenance of the peculiar paths of energy and nutrient-mobilization in these pristine ecosystems, which are vulnerable to threats by the joint action of abiotic stressors related to global change. ; This research was supported by Junta de Andalucía (Excelencia P07-CVI-02598 to PC, and P09-RNM-5376 to JMMS), the Spanish Ministries of Medio Ambiente, Rural y Marino (PN2009/067 to PC) and Ciencia e Innovación (GLC2008-01127/BOS and CGL2011-23681 to PC), the ERC Advanced Grant project number 250254 "MINOS" (to GB), and two Spanish government grants (to JADM and FJB).

Global change, together with human activities, has resulted in increasing amounts of organic material (including nutrients) that water bodies receive. This input further attenuates the penetration of solar radiation, leading to the view that opaque lakes are more "protected" from solar ultraviolet radiation (UVR) than clear ones. Vertical mixing, however, complicates this view as cells are exposed to fluctuating radiation regimes, for which the effects have, in general, been neglected. Furthermore, the combined impacts of mixing, together with those of UVR and nutrient inputs are virtually unknown. In this study, we carried out complex in situ experiments in three high mountain lakes of Spain (Lake Enol in the National Park Picos de Europa, Asturias, and lakes Las Yeguas and La Caldera in the National Park Sierra Nevada, Granada), used as model ecosystems to evaluate the joint impact of these climate change variables. The main goal of this study was to address the question of how short-term pulses of nutrient inputs, together with vertical mixing and increased UVR fluxes modify the photosynthetic responses of phytoplankton. The experimentation consisted in all possible combinations of the following treatments: (a) solar radiation: UVR + PAR (280–700 nm) versus PAR (photosynthetically active radiation) alone (400–700 nm); (b) nutrient addition (phosphorus (P) and nitrogen (N)): ambient versus addition (P to reach to a final concentration of 30 μg P L−1, and N to reach N:P molar ratio of 31); and (c) mixing: mixed (one rotation from surface to 3 m depth (speed of 1 m 4 min−1, total of 10 cycles)) versus static. Our findings suggest that under ambient nutrient conditions there is a synergistic effect between vertical mixing and UVR, increasing phytoplankton photosynthetic inhibition and excretion of organic carbon (EOC) from opaque lakes as compared to algae that received constant mean irradiance within the epilimnion. The opposite occurs in clear lakes where antagonistic effects were determined, with mixing partially counteracting the negative effects of UVR. Nutrient input, mimicking atmospheric pulses from Saharan dust, reversed this effect and clear lakes became more inhibited during mixing, while opaque lakes benefited from the fluctuating irradiance regime. These climate change related scenarios of nutrient input and increased mixing, would not only affect photosynthesis and production in lakes, but might also further influence the microbial loop and trophic interactions via enhanced EOC under fluctuating UVR exposure. ; This work was supported by Ministerio Español de Medio Ambiente, Rural y Marino (PN2009/067) and Ciencia e Innovación (GLC2008-01127/BOS and CGL2011-23681), Junta de Andalucía (Excelencia CVI-02598), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2007-1651) and Fundación Playa Unión; GH and CD were supported by the Spanish Government – Formación de Profesorado Universitario Grant.