Atmo-ecometabolomics: a novel atmospheric particle chemical characterization methodology for ecological research

Rivas-Ubach A., Liu Y., Steiner A.L., Sardans J., Tfaily M.M., Kulkarni G., Kim Y.-M., Bourrianne E., Paša-Tolić L., Peñuelas J., Guenther A. (2019) Atmo-ecometabolomics: a novel atmospheric particle chemical characterization methodology for ecological research. Environmental Monitoring and Assessment. 191: 0-0.
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Doi: 10.1007/s10661-019-7205-x

Resumen:

Aerosol particles play important roles in processes controlling the composition of the atmosphere and function of ecosystems. A better understanding of the composition of aerosol particles is beginning to be recognized as critical for ecological research to further comprehend the link between aerosols and ecosystems. While chemical characterization of aerosols has been practiced in the atmospheric science community, detailed methodology tailored to the needs of ecological research does not exist yet. In this study, we describe an efficient methodology (atmo-ecometabolomics), in step-by-step details, from the sampling to the data analyses, to characterize the chemical composition of aerosol particles, namely atmo-metabolome. This method employs mass spectrometry platforms such as liquid and gas chromatography mass spectrometries (MS) and Fourier transform ion cyclotron resonance MS (FT-ICR-MS). For methodology evaluation, we analyzed aerosol particles collected during two different seasons (spring and summer) in a low-biological-activity ecosystem. Additionally, to further validate our methodology, we analyzed aerosol particles collected in a more biologically active ecosystem during the pollination peaks of three different representative tree species. Our statistical results showed that our sampling and extraction methods are suitable for characterizing the atmo-ecometabolomes in these two distinct ecosystems with any of the analytical platforms. Datasets obtained from each mass spectrometry instrument showed overall significant differences of the atmo-ecometabolomes between spring and summer as well as between the three pollination peak periods. Furthermore, we have identified several metabolites that can be attributed to pollen and other plant-related aerosol particles. We additionally provide a basic guide of the potential use ecometabolomic techniques on different mass spectrometry platforms to accurately analyze the atmo-ecometabolomes for ecological studies. Our method represents an advanced novel approach for future studies in the impact of aerosol particle chemical compositions on ecosystem structure and function and biogeochemistry. © 2019, Springer Nature Switzerland AG.

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We are what we eat: A stoichiometric and ecometabolomic study of caterpillars feeding on two pine subspecies of Pinus sylvestris

Rivas-Ubach A., Peñuelas J., Hódar J.A., Oravec M., Paša-Tolić L., Urban O., Sardans J. (2019) We are what we eat: A stoichiometric and ecometabolomic study of caterpillars feeding on two pine subspecies of Pinus sylvestris. International Journal of Molecular Sciences. 20: 0-0.
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Doi: 10.3390/ijms20010059

Resumen:

Many studies have addressed several plant-insect interaction topics at nutritional, molecular, physiological, and evolutionary levels. However, it is still unknown how flexible the metabolism and the nutritional content of specialist insect herbivores feeding on different closely related plants can be. We performed elemental, stoichiometric, and metabolomics analyses on leaves of two coexisting Pinus sylvestris subspecies and on their main insect herbivore; the caterpillar of the processionary moth (Thaumetopoea pityocampa). Caterpillars feeding on different pine subspecies had distinct overall metabolome structure, accounting for over 10% of the total variability. Although plants and insects have very divergent metabolomes, caterpillars showed certain resemblance to their plant-host metabolome. In addition, few plant-related secondary metabolites were found accumulated in caterpillar tissues which could potentially be used for self-defense. Caterpillars feeding on N and P richer needles had lower N and P tissue concentration and higher C:N and C:P ratios, suggesting that nutrient transfer is not necessarily linear through trophic levels and other plant-metabolic factors could be interfering. This exploratory study showed that little chemical differences between plant food sources can impact the overall metabolome of specialist insect herbivores. Significant nutritional shifts in herbivore tissues could lead to larger changes of the trophic web structure. © 2018 by the authors. Licensee MDPI, Basel, Switzerland.

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Coping with iron limitation: a metabolomic study of Synechocystis sp. PCC 6803

Rivas-Ubach A., Poret-Peterson A.T., Peñuelas J., Sardans J., Pérez-Trujillo M., Legido-Quigley C., Oravec M., Urban O., Elser J.J. (2018) Coping with iron limitation: a metabolomic study of Synechocystis sp. PCC 6803. Acta Physiologiae Plantarum. 40: 0-0.
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Doi: 10.1007/s11738-018-2603-1

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Iron (Fe) is a key element for all living systems, especially for photosynthetic organisms because of its important role in the photosynthetic electron transport chain. Fe limitation in cyanobacteria leads to several physiological and morphological changes. However, the overall metabolic responses to Fe limitation are still poorly understood. In this study, we integrated elemental, stoichiometric, macromolecular, and metabolomic data to shed light on the responses of Synechocystis sp. PCC 6803, a non-N2-fixing freshwater cyanobacterium, to Fe limitation. Compared to Synechocystis growing at nutrient replete conditions, Fe-limited cultures had lower growth rates and amounts of chlorophyll a, RNA, RNA:DNA, C, N, and P, and higher ratios of protein:RNA, C:N, C:P, and N:P, in accordance with the growth rate hypothesis which predicts faster growing organisms will have decreased biomass RNA contents and C:P and N:P ratios. Fe-limited Synechocystis had lower amounts Fe, Mn, and Mo, and higher amount of Cu. Several changes in amino acids of cultures growing under Fe limitation suggest nitrogen limitation. In addition, we found substantial increases in stress-related metabolites in Fe-limited cyanobacteria such antioxidants. This study represents an advance in understanding the stoichiometric, macromolecular, and metabolic strategies that cyanobacteria use to cope with Fe limitation. This information, moreover, may further understanding of changes in cyanobacterial functions under scenarios of Fe limitation in aquatic ecosystems. © 2018, Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków.

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Impacts of global change on Mediterranean forests and their services

Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino-Serrano, M., Vives-Ingla, M., Stocker, B.D., Balzarolo, M., Guerrieri, R., Peaucelle, M., Marañón-Jiménez, S., Bórnez-Mejías, K., Mu, Z., Descals, A., Castellanos, A., Terradas, J. (2017) Impacts of global change on Mediterranean forests and their services. Forests. 8: 0-0.
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Doi: 10.3390/f8120463

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Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia

Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Rico, L., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino, M., Vives, M., Nadal-Sala, D., Sabaté, S., Gracia, C., Terradas, J. (2016) Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environmental and Experimental Botany. : 0-0.
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Doi: 10.1016/j.envexpbot.2017.05.012

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Topsoil depth substantially influences the responses to drought of the foliar metabolomes of Mediterranean forests

Rivas-Ubach A., Barbeta A., Sardans J., Guenther A., Ogaya R., Oravec M., Urban O., Peñuelas J. (2016) Topsoil depth substantially influences the responses to drought of the foliar metabolomes of Mediterranean forests. Perspectives in Plant Ecology, Evolution and Systematics. 21: 41-54.
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Doi: 10.1016/j.ppees.2016.06.001

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The upper soil provides support, water, and nutrients to terrestrial plants and is therefore crucial for forest dynamics. We hypothesised that a tree's metabolic activity (and therefore its metabolome; the total set of metabolites) would be affected by both the depth of upper soil layers and water availability. We sampled leaves for stoichiometric and metabolomic analyses once per season from differently sized Quercus ilex trees under natural and experimental drought conditions representing the likely conditions in the coming decades). Although the metabolomes varied according to tree size, smaller trees did not show higher concentrations of biomarker metabolites related to drought stress. However, the effect of the drought treatment on the metabolomes was greatest for small trees growing in shallow soils. Our results suggest that tree size is more dependent on the depth of the upper soil, which indirectly affects a tree's metabolome, rather than on the moisture content in the upper soil. Metabolomic profiling of Q. ilex supports our finding that water availability in the upper soil is not necessarily correlated with tree size. The higher impact of drought on trees growing in shallower soils nevertheless indicates that any increase in the frequency, intensity, and duration of drought - as has been projected for the Mediterranean Basin and other areas - would affect small trees most. Metabolomics has proved to be a useful means for investigating the links between plant metabolism and environmental conditions. © 2016.

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Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant–folivore coevolutionary processes?

Rivas-Ubach A., Hódar J.A., Sardans J., Kyle J.E., Kim Y.-M., Oravec M., Urban O., Guenther A., Peñuelas J. (2016) Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant–folivore coevolutionary processes?. Ecology and Evolution. 6: 4372-4386.
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Doi: 10.1002/ece3.2206

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The debate whether the coevolution of plants and insects or macroevolutionary processes (phylogeny) is the main driver determining the arsenal of molecular defensive compounds of plants remains unresolved. Attacks by herbivorous insects affect not only the composition of defensive compounds in plants but also the entire metabolome. Metabolomes are the final products of genotypes and are constrained by macroevolutionary processes, so closely related species should have similar metabolomic compositions and may respond in similar ways to attacks by folivores. We analyzed the elemental compositions and metabolomes of needles from three closely related Pinus species with distant coevolutionary histories with the caterpillar of the processionary moth respond similarly to its attack. All pines had different metabolomes and metabolic responses to herbivorous attack. The metabolomic variation among the species and the responses to folivory reflected their macroevolutionary relationships, with P. pinaster having the most divergent metabolome. The concentrations of terpenes were in the attacked trees supporting the hypothesis that herbivores avoid plant individuals with higher concentrations. Our results suggest that macroevolutionary history plays important roles in the metabolomic responses of these pine species to folivory, but plant–insect coevolution probably constrains those responses. Combinations of different evolutionary factors and trade-offs are likely responsible for the different responses of each species to folivory, which is not necessarily exclusively linked to plant–insect coevolution. © 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

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Morphological, biochemical and physiological traits of upper and lower canopy leaves of European beech tend to converge with increasing altitude

Rajsnerova P., Klem K., Holub P., Novotna K., Vecerova K., Kozacikova M., Rivas-Ubach A., Sardans J., Marek M.V., Penuelas J., Urban O. (2015) Morphological, biochemical and physiological traits of upper and lower canopy leaves of European beech tend to converge with increasing altitude. Tree Physiology. 35: 47-60.
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Doi: 10.1093/treephys/tpu104

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The present work has explored for the first time acclimation of upper versus lower canopy leaves along an altitudinal gradient. We tested the hypothesis that restrictive climatic conditions associated with high altitudes reduce within-canopy variations of leaf traits. The investigated beech (Fagus sylvatica L.) forest is located on the southern slope of the Hrubý Jeseník Mountains (Czech Republic). All measurements were taken on leaves from upper and lower parts of the canopy of mature trees (>85 years old) growing at low (400 m above sea level, a.s.l.), middle (720 m a.s.l.) and high (1100 m a.s.l.) altitudes. Compared with trees at higher altitudes, those growing at low altitudes had lower stomatal conductance, slightly lower CO2 assimilation rate (A max) and leaf mass per area (LMA), and higher photochemical reflectance index, water-use efficiency and Rubisco content. Given similar stand densities at all altitudes, the different growth conditions result in a more open canopy and higher penetration of light into lower canopy with increasing altitude. Even though strong vertical gradients in light intensity occurred across the canopy at all altitudes, lower canopy leaves at high altitudes tended to acquire the same morphological, biochemical and physiological traits as did upper leaves. While elevation had no significant effect on nitrogen (N) and carbon (C) contents per unit leaf area, LMA, or total content of chlorophylls and epidermal flavonoids in upper leaves, these increased significantly in lower leaves at higher altitudes. The increases in N content of lower leaves were coupled with similar changes in A max. Moreover, a high N content coincided with high Rubisco concentrations in lower but not in upper canopy leaves. Our results show that the limiting role of light in lower parts of the canopy is reduced at high altitudes. A great capacity of trees to adjust the entire canopy is thus demonstrated. © © The Author 2015. Published by Oxford University Press. All rights reserved.

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Similar local, but different systemic, metabolomic responses of closely related pine subspecies to folivory by caterpillars of the processionary moth

Rivas-Ubach A., Sardans J., Hódar J.A., Garcia-Porta J., Guenther A., Oravec M., Urban O., Peñuelas J. (2015) Similar local, but different systemic, metabolomic responses of closely related pine subspecies to folivory by caterpillars of the processionary moth. Plant Biology. : 0-0.
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Doi: 10.1111/plb.12422

Resumen:

Plants respond locally and systemically to herbivore attack. Most of the research conducted on plant-herbivore relationships at element and molecular levels have focused on the elemental composition or/and certain molecular compounds or specific families of defence metabolites showing that herbivores tend to select plant individuals or species with higher nutrient concentrations and avoid those with higher levels of defence compounds. We performed stoichiometric and metabolomics, both local and systemic, analyses in two subspecies of Pinus sylvestris under attack from caterpillars of the pine processionary moth, an important pest in the Mediterranean Basin. Both pine subspecies responded locally to folivory mainly by increasing relative concentrations of terpenes and some phenolics. Systemic responses differed between pine subspecies, and most of the metabolites presented intermediate concentrations between those of the affected parts and unattacked trees. Our results support the hypothesis that foliar nutrient concentrations are not a key factor for plant selection by adult female processionary moths for oviposition, since folivory was not associated with any of the elements analysed. Phenolic compounds generally did not increase in the attacked trees, questioning the suggestion of induction of phenolics following folivory attack and the anti-feeding properties of phenolics. Herbivory attack produced a general systemic shift in pines, in both primary and secondary metabolism, which was less intense and chemically different from the local responses. Local pine responses were similar between pine subspecies, while systemic responses were more distant. © 2015 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Opposite metabolic responses of shoots and roots to drought

Gargallo-Garriga A., Sardans J., Pérez-Trujillo M., Rivas-Ubach A., Oravec M., Vecerova K., Urban O., Jentsch A., Kreyling J., Beierkuhnlein C., Parella T., Peñuelas J. (2014) Opposite metabolic responses of shoots and roots to drought. Scientific Reports. 4: 0-0.
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Doi: 10.1038/srep06829

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Shoots and roots are autotrophic and heterotrophic organs of plants with different physiological functions. Do they have different metabolomes? Do their metabolisms respond differently to environmental changes such as drought? We used metabolomics and elemental analyses to answer these questions. First, we show that shoots and roots have different metabolomes and nutrient and elemental stoichiometries. Second, we show that the shoot metabolome is much more variable among species and seasons than is the root metabolome. Third, we show that the metabolic response of shoots to drought contrasts with that of roots; shoots decrease their growth metabolism (lower concentrations of sugars, amino acids, nucleosides, N, P, and K), and roots increase it in a mirrored response. Shoots are metabolically deactivated during drought to reduce the consumption of water and nutrients, whereas roots are metabolically activated to enhance the uptake of water and nutrients, together buffering the effects of drought, at least at the short term.

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