Philippa Kaur

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Acrylic and polydimethylsiloxane (PDMS) molds preparationThe incubating device for the porous microplate was designed using a CAD software (Solidworks, Dassault Systèmes) and the exported drawing files were used to laser cut 1/4” and 1/8” acrylic sheet (Universal Laser Systems; Supplementary Fig. S2). After washing the cut acrylic parts with deionized water, they were attached by acrylic (Weld-On) and epoxy (3 M) adhesives that were followed by a curing process for ~18 h. Polydimethylsiloxane (PDMS) (Sylgard 184, Dow Corning) was cast onto the acrylic mold and cured at 80 °C for at least 3 h. The PDMS mold was carefully detached from the acrylic surface by dispensing isopropyl alcohol (VWR) into the area between the PDMS and the acrylic molds (Fig. 2a).Fig. 2: Synthesis and characterization of porous microplate.a Procedure to build a porous microplate using polydimethylsiloxane (PDMS) and acrylic molds. b Image of the microplate with an array of culture wells (wall thickness: 0.9 mm). c Scanning electron microscopy image of nanoporous copolymer HEMA–EDMA.Full size imagePorous microplate preparationSynthesis of copolymer HEMA–EDMA was based on previously described protocols [30, 31] and details are given as follows. Prepolymer solution HEMA − EDMA was prepared by mixing 2-hydroxyethyl methacrylate (HEMA; monomer, 24 wt.%, Sigma-Aldrich), ethylene glycol dimethacrylate (EDMA; crosslinker, 16 wt.%, Sigma-Aldrich), 1-decanol (porogen, 12 wt.%, Sigma-Aldrich), cyclohexanol (porogen, 48 wt.%, Sigma-Aldrich) and 2,2-dimethoxy-2-phenylacetophenone (DMPAP; photoinitiator, 1 wt.%). The solution was stored at room temperature without light exposure until further use. Glass slides (75 × 50 mm2, VWR) were chemically cleaned by sequentially soaking in 1 M hydrochloric acid and 1 M sodium hydroxide for one hour, followed by rinsing with deionized water and air drying. The prepolymer solution was cast onto the PDMS mold and a glass slide was placed on the mold. The solution was then polymerized under ultraviolet light with a wavelength 365 nm for 15 min by using a commercial UV lamp (VWR). The photopolymerized device was detached from the PDMS mold and stored in a jar containing methanol (VWR) until further use (Fig. 2a). The jar was refilled with new methanol twice in order to remove the remaining porogen and uncrosslinked monomers from the hydrogel.Upon each incubation experiment with the porous microplate, each device was decontaminated by replacing the solvent with 70% alcohol (VWR) and storing it for 24 h. They were immersed in a pre-autoclaved jar for two weeks with f/2 medium with omitted silicate, where the jar was refilled once with a new sterile medium to adjust its pH for the algal culture and remove any solvent remaining in the hydrogel. Before inoculating microbial cells, each microplate was taken out from the jar and the media remaining on the top surface was removed by absorbing it with a pre-sterilized wipe to minimize the chance for cross-contamination between wells (Fig. 2b).Scanning electron microscopyPhotopolymerized HEMA − EDMA was removed from methanol and dried in air for at least one week to evaporate the excess solvent. A ~5 × 5 mm2 specimen was collected from the dried copolymer and attached to a pin stub. The stub was loaded on a scanning electron microscope (SEM; MERLIN, Carl Zeiss), and the specimen was characterized with imaging software (SmartSEM, Carl Zeiss) with 16,270X magnification and an operating voltage of 1 kV. The SEM imaging was performed at the Electron Microscopy Facility in the MIT Materials Research Science and Engineering Centers (MRSEC; Fig. 2c).Strains and culturing conditionsAxenic P. tricornutum CCMP 2561 was acquired from the National Center for Marine Algae and Microbiota (NCMA) and shown to be axenic via epifluorescence microscopy and sequencing of the 16 S rRNA gene [11]. P. tricornutum was maintained in f/2 medium with 20 g L−1 commercially available sea salts (Instant Ocean, Blacksburg) and with omitted silicate, which we will refer to as f/2-Si [11, 16]. Batch cultures were grown at 20 °C with a 12 h light/12 h dark diurnal cycle and a light intensity of 200 μmol photons m−2 s−1 (Exlenvce). Every 2–3 weeks, axenic cultures were monitored for bacterial contamination by streaking culture samples on marine broth agar [33], that tests for contamination by bacteria that can grow on agar media and is not definitive. Every 6–12 months, every axenic and bacterial co-culture of P. tricornutum was inspected for the absence/presence of bacteria by staining the cellular DNA with 0.1% v/v SYTO BC Green Fluorescent Acid Stain (Thermofisher, Supplementary Fig. S1).Bacterial community samples (referred to as “phycosphere enrichments”) were obtained from mesocosms of P. tricornutum and maintained as previously described [11, 16]. Briefly, an outdoor P. tricornutum mesocosm sample in natural seawater was collected in Corpus Christi, TX and filtered with 0.6–1 µm pores to remove larger algal cells. The bacterial filtrates were inoculated to an axenic algal culture, maintained in f/2-Si media for ~3 months, and washed with a sterile medium to enrich for phycosphere-associated bacteria. These enriched communities were subsequently co-cultured with P. tricornutum in f/2-Si media for ~4 years prior to the start of the experiments.Two bacterial strains, Marinobacter sp. 3-2 and Algoriphagus sp. ARW1R1, were isolated from the phycosphere enrichment samples (Supplementary Table S1). The isolates were either maintained by growing on marine broth agar plates at 30 °C or by co-culturing with P. tricornutum through inoculation of a single colony into the axenic culture.
P. tricornutum culture in porous microplateThree baseline experiments were designed to study how the alga P. tricornutum interacts with its associated bacteria in the porous microplate (Fig. 1). For experiments assessing the algal growth in the microplate, axenic P. tricornutum was acclimated to a copolymer environment in advance by inoculating a stationary phase-culture to a separate microplate. After acclimation for 4 days, the culture was diluted to ~1 × 106 cells ml−1 and transferred to the experimental microplate. Three replicated microplates were placed in a single transparent covered container (128 × 85 × 10 mm3, VWR) which was filled with ~25 ml f/2-Si medium to keep the microplate hydrated throughout the incubation period of 20 days with an initial culture volume of 75 µl (Fig. 1a). The procedures were conducted under a biosafety cabinet to prevent any biological contamination. The cells were incubated under the same conditions as described above for the batch cultures (temperature, light intensity, diurnal cycle).Growth of P. tricornutum was measured by counting cells using a hemocytometer (Electron Microscopy Sciences) or flow cytometry (described later). Specific growth rates were calculated from the natural log of the cell densities in triplicate sampled during an exponential growth phase (day 3 for the batch culture, day 5 for the porous microplate system; Fig. 3a).Fig. 3: Cultivation of P. tricornutum in the porous microplate.a Schematic of a microplate for algal cultivation. b Growth curve and maximal growth rate (inset) comparing the porous microplate with flask culture. Error bars, standard deviation of triplicates. c Cell abundance at center (n = 3) and surrounding (n = 18) wells after incubation. Asterisks denote statistical differences with following levels (two-tailed t-test): ***P  More

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Plant and fruit characteristicsBiometric parameters of plantsThe analyzed cultivars (characterized by desirable morphological, physical and chemical properties, uniform ripening, suitability for mechanical harvesting, high productivity, resistance to diseases and pests) and the application of modern farming technologies can have significant effects on crop yields and quality and, in consequence, production profitability, which was also observed by other authors11,23,24,25.The influence of the combined application of biostimulants on the biometric parameters of plants in the analyzed cultivars of C. annuum is presented in Table 1. The analyzed biostimulants had no significant effect on the values of leaf greenness (SPAD), relative to the control treatment. In the tested cultivars, the mean values of this parameter ranged from 52.5 (cv. ‘Turbine F1’) to 58.8 (cv. ‘Cyklon’). In general, leaf greenness was not significantly affected by the treatment × cultivar interaction, although two homogeneous groups were identified: cvs. ‘Turbine F1’ and ‘Palivec’, and cvs. ‘Solario F1’, ‘Whitney F1’ and ‘Cyklon’.Table 1 Effect of the combined application of biostimulants on the biometric parameters (mean values ± standard deviations) of plants in the analyzed cultivars of Capsicum.Full size tableThe average weight of aboveground plant parts ranged from 112 g (cv. ‘Palivec’) to 248 g (cv. ‘Solario F1’), and average root weight ranged from 112 g (cv. ‘Palivec’) to 220 g (cv. ‘Cyklon’). These parameters were not significantly affected by the method of biostimulant application, but their values were highest in treatment I (combined application of BB Soil, BB Foliar and Multical). The analyzed C. annuum cultivars can be divided into three homogeneous groups based on the weight of aboveground plant parts, and into two homogeneous groups based on root weight, but the biostimulants exerted different effects on these parameters in each cultivar. The weight of aboveground plant parts was highest in cv. ‘Solario F1’ in treatments I and III, and lowest in cv. ‘Palivec’ in treatment III. Root weight was highest in cv. ‘Cyklon’ in treatment I, and lowest in cv. ‘Palivec’ in the control treatment.It can be concluded that the combined application of the tested biostimulants had a minor effect on the biometric parameters of pepper plants. In contrast, Thevanathan et al.26 and Bai et al.27 demonstrated that algal extracts had a considerable influence on plant height (35% increase) in pulses. Bilal28, Abou-Shlell et al.29 and Hamed30 found that the natural foliar nano-fertilizer Lithovit positively affected the vegetative growth of crop plants.YieldThe fruit yields of the analyzed C. annuum cultivars treated with biostimulants applied in different combinations are presented in Table 2. Similarly to the values of leaf greenness and biometric parameters of plants, early, marketable and total yields were determined mostly by varietal traits, whereas biostimulants exerted a minor effect. On average, ‘Whitney F1’ was the highest-yielding cultivar, and ‘Cyklon’ was the lowest-yielding cultivar. Sweet cultivars were characterized by higher yields than hot cultivars, and the best results were noted in treatment II (combined application of BB Soil, BB Foliar, Multical and MK5), although no significant differences were observed relative to the control treatment and the remaining experimental treatments. The early yield ranged from 0.2 kg·m−2 (cv. ‘Cyklon’) to 3.8 kg·m−2 (cv. ‘Whitney F1’), and ‘Cyklon’ and ‘Palivec’ (hot cultivars) were characterized by similar early yields. The marketable yield was lowest in cv. ‘Cyklon’ (3.1 kg·m−2) and highest in cv. ‘Turbine F1’ (7.3 kg·m−2). ‘Turbine F1’ and ‘Whitney F1’ were characterized by comparable marketable yields. Similar effects were observed with regard to total yield. An analysis of the values of marketable and total yields revealed that the percentage of marketable fruits was higher in hot cultivars (approx. 100% on average) than in sweet cultivars (approx. 93–99% on average), and it was lowest in cv. ‘Whitney F1’ in treatment II (combined application of BB Soil, BB Foliar, Multical and MK5)—around 88%. The analyzed C. annuum cultivars responded differently to the tested combinations of biostimulants in terms of yield, but they did not differ significantly in total fruit yield, although nine homogeneous groups were identified.Table 2 Effect of the combined application of biostimulants on fruit yield (mean values ± standard deviations) in the analyzed cultivars of Capsicum annuum.Full size tableA positive effect of titanium application on crop yields was also observed by Marcinek and Hetman31 in Sparaxis tricolor Ker Gawl, and by Grajkowski and Ochmian32 in raspberries. In a study of strawberries conducted by Michalski33, the effectiveness of titanium in plant nutrition varied across years. Dobromilska34 reported that the foliar application of titanium contributed to an increase in tomato yields and significantly enhanced the vegetative growth of tomato plants, including an increase in plant height, stem diameter and the number of leaves per plant. Normal vegetative growth and development contributes to improving crop quality, and genetic factors play a major role under identical growing conditions6.Biometric parameters of fruitThe biometric parameters of fruit in the analyzed C. annuum cultivars are presented in Table 3. Similarly to the previously described traits, the biometric parameters of pepper fruit were not significantly influenced by the tested biostimulants. The biometric parameters of fruits were affected by varietal traits, and differences were noted between sweet and hot cultivars. The fruits of sweet cultivars had higher weight, larger horizontal diameter, thicker skin and smaller vertical diameter, compared with hot cultivars. No significant treatment × cultivar interaction was found for the weight, vertical diameter or horizontal diameter of fruit, although several homogeneous groups could be identified based on the differences between cultivars.Table 3 Effect of the combined application of biostimulants on the biometric parameters (mean values ± standard deviations) of fruit in the analyzed cultivars of Capsicum annuum.Full size tableAverage fruit weight varied widely across cultivars, from 39 g (cv. ‘Cyklon’) to 224 g (cv. ‘Solario F1’). Hot cultivars (‘Cyklon’ and ‘Palivec’) formed a homogeneous group based on fruit weight. The fruit weight in hot cultivars of C. annuum was similar to that reported by Islam et al.24. Sweet and hot pepper cultivars differ also in fruit shape. The fruits of hot cultivars are long and narrow, whereas the fruits of sweet cultivars have similar horizontal and vertical dimeters. Sweet cultivars are similar in terms of vertical diameter, and they differ mostly in average horizontal diameter. Fruits with the smallest mean vertical diameter (9.1 cm) were harvested from plants of cv. ‘Turbine F1’, and fruits with the largest mean vertical diameter (14.6 cm) were harvested from plants of cv. ‘Palivec’. Fruits with the smallest mean horizontal diameter (2.4 cm) were harvested from plants of cv. ‘Palivec’, and fruits with the largest mean horizontal diameter (9.0 cm) were harvested from plants of cv. ‘Solario F1’.The fruits of sweet and hot C. annuum cultivars had pericarps of similar thickness. In hot cultivars, average skin thickness ranged from 2.9 mm (cv. ‘Palivec’) to 3.3 mm (cv. ‘Cyklon’), and in sweet cultivars—from 5.7 mm (cv.‘Turbine F1’) to 6.4 mm (cv. ‘Whitney F1’).Chemical composition of fruitThe proximate chemical composition of fruit in the analyzed C. annuum cultivars is presented in Table 4. The effects exerted by biostimulants on most chemical properties of pepper fruit (excluding L-ascorbic acid content) varied across cultivars. The applied biostimulants led to both an increase and a decrease in the content of the analyzed components in the studied cultivars. No significant differences in the concentrations of dry matter, total sugars, reducing sugars or L-ascorbic acid in pepper fruit were found between treatments. In comparison with the control treatment, significant differences were noted only for nitrate (V) levels in treatment I. The combined application of biostimulants led to an increase in the nitrate (V) content of fruit, which was nearly two-fold higher in treatment I than in the control group. The fruits of sweet cultivars had a lower content of dry matter, total sugars and L-ascorbic acid than the fruits of hot cultivars.Table 4 Effect of the combined application of biostimulants on the chemical composition (mean values ± standard deviations) of fruit in the analyzed cultivars of Capsicum annuum.Full size tableAverage dry matter content ranged from 6.4% (cv. ‘Whitney F1’) to 7.6% (cv. ‘Solario F1’) in sweet peppers, and from 11.6% (cv. ‘Cyklon’) to 12.3% (cv. ‘Cyklon’) in hot peppers. Sweet and hot cultivars of C. annuum formed separate homogeneous groups. The analyzed cultivars differed significantly in the total sugar content of fruit, which was lowest in cv. ‘Whitney F1’ and highest in cv. ‘Cyklon’. Average total sugar content ranged from 3.2 to 4.6 g∙100 g−1 fresh weight in sweet peppers, and from 6.9 to 8.4 g∙100 g−1 fresh weight in hot peppers. Cultivars ‘Whitney F1’, ‘Turbine F1’ and ‘Palivec’, and ‘Solario F1’ and ‘Palivec’ formed homogeneous groups based on the reducing sugar content of fruit, which ranged from 2.4 g∙100 g−1 fresh weight (cv. ‘Whitney F1’ and ‘Turbine F1’) to 5.1 g∙100 g−1 fresh weight (cv. ‘Cyklon’). Average L-ascorbic acid content 97 mg∙100 g−1 fresh weight in sweet peppers, and 107 mg∙100 g−1 fresh weight in hot peppers. Similarly to the dry matter content of fruit, separate homogeneous groups were formed by sweet and hot cultivars of C. annuum. The combined application of biostimulants caused an increase in the average nitrate (V) content of pepper fruit, which ranged from 136 mg N-NO3 kg−1 fresh weight (cv. ‘Palivec’) to 259 mg N-NO3 kg−1 fresh weight (cv. ‘Turbine F1’).According to Selahle et al.35, the taste of sweet peppers is determined by the content of sugars and organic acids. Taste is a complex phenomenon, and it is affected by environmental factors during plant growth36,37. From the nutritional perspective, the dry matter of pepper fruit consists of sugars, organic acids and other compounds with proven nutraceutical efficacy, including hydrophilic compounds such as ascorbic acid, flavonoids and phenolic acids, and lipophilic compounds such as carotenoids and tocopherols38,39,40,41. Fresh peppers are rich in valuable compounds including vitamins (in particular vitamin C), mineral salts, macronutrients and micronutrients42. According to Hallmann et al.43, pepper fruit contains on average 8.5–10.5 g 100 g fresh weight of dry matter, 3.6–6.6 g 100 g fresh weight of total sugars, 2.4–4.8 g 100 g fresh weight of reducing sugars, and 115–153 mg 100 g fresh weight of L-ascorbic acid, depending on cultivation method. Similar values were determined in the present study. The content of nitrates (V) depends on soil and climatic conditions, fertilization and plant species44, which were identical in all treatments in this study. The tested biostimulants exerted varied effects on the nutrient content of C. annuum fruit. The nitrate (V) content of fruit was higher in experimental treatments than in the control group, but the noted differences were significant only relative to treatment I where the maximum permissible level of 250 mg N-NO3 kg−1 fresh weight was exceeded43. ‘Turbine F1’, followed by ‘Solario F1’, were most prone to nitrate (V) accumulation in fruit. In this respect, the effect exerted by the biostimulants was undesirable.Correlations between the analyzed biometric parameters and chemical composition of fruitDue to the fact that the tested biostimulants exerted no clear-cut effects on the analyzed biometric parameters of C. annuum fruit, and for the sake of simplicity, the measurement data were pooled into two experimental groups of sweet and hot cultivars. The results of a correlation analysis of the above parameters are presented in Table 5. The absolute values of the correlation coefficient ranged from 0.012 (correlation between the L-ascorbic acid content and nitrate (V) content of fruit in sweet cultivars) to 0.932 (correlation between the weight and horizontal diameter of fruit in sweet cultivars). Significant correlations were noted in 36 cases out of 72 comparisons, whereas practical significance (coefficient of correlation minimum 0.4) was observed in 33 comparisons. The nitrate (V) content of fruit was least frequently correlated, and the horizontal diameter, total sugar content and reducing sugar content of fruit were most frequently correlated with the remaining parameters. The nature of relationships between the analyzed parameters was largely affected by the type of cultivar. Differences in the significance of correlation coefficients were found in 19 pairs of the compared traits, and differences in their direction (positive, negative) were observed in 11 pairs out of 36 comparisons. The significance and direction of correlations were consistent only with regard to horizontal diameter vs. the total sugar content and reducing sugar content, and skin thickness vs. reducing sugar content and L-ascorbic acid content. This implies that irrespective of cultivar, an increase in the horizontal diameter of fruit was associated with an increase in sugar content, and an increase in skin thickness was associated with an increase in the content of reducing sugars and L-ascorbic acid. Therefore, it can be assumed that the fruits characterized by a larger horizontal diameter and thicker skin are richer in nutrients.Table 5 Pearson’s coefficients of correlation between the analyzed parameters of Capsicum annuum fruit.Full size tableIn the group of fruit biometric parameters, the strongest correlation was found between the horizontal diameter and weight of fruit in sweet cultivars (coefficient of determination R2 = 0.87), and it was well described by a linear function (Fig. 1a). An increase in the horizontal diameter of fruit from around 4.7 cm to around 10.2 cm was accompanied by a proportional increase in fruit weight from around 53 g to around 254 g (by approx. 380%). Equations with the minimum value of the determination coefficient (0.4) were also derived for the correlations between the vertical diameter and weight of fruit, and between the horizontal diameter and skin thickness of fruit in hot cultivars (Figs. 1b and 1c). An increase in the vertical diameter of fruit by around 65% increased their weight by around 40%, and an increase in the horizontal diameter of fruit by around 120% increased their skin thickness by around 40%.Figure 1Relationships between the biometric parameters of Capsicum annuum fruit: (a) horizontal diameter and weight of sweet peppers, (b) vertical diameter and weight of hot peppers, (c) horizontal diameter and skin thickness of hot peppers.Full size imageThe biometric parameters and chemical composition of pepper fruit are strongly correlated (Figs. 2 and 3). Three and six equations with the minimum value of the determination coefficient (0.4) were derived for the correlations between fruit parameters in sweet and hot pepper cultivars, respectively. In sweet cultivars, the dry matter content of fruit was affected by their weight and horizontal diameter, and the noted relationships were directly proportional. An increase in fruit weight by around 360% (Fig. 2a) and an increase in the horizontal diameter of fruit by around 115% (Fig. 2c) increased their dry matter content by around 35%. An increase in the vertical diameter of fruit by around 60% increased their L-ascorbic acid content by around 25% (Fig. 2b). In hot cultivars, the chemical composition of fruit was most significantly influenced by horizontal diameter, followed by skin thickness. An increase in the horizontal diameter of fruit from around 2.0 cm to around 4.5 cm was accompanied by an increase in their total sugar content by around 50% (from approx. 6.5 g∙100 g−1 fresh weight to approx. 9.8 g∙100 g−1 fresh weight) (Fig. 3b), reducing sugar content—by around 100% (from approx. 3.0 g∙100 g−1 fresh weight to approx. 6.1 g∙100 g−1 fresh weight) (Fig. 3c) and nitrate (V) content—by around 80% (from approx. 125 mg N-NO3 kg−1 fresh weight to approx. 228 mg N-NO3 kg−1 fresh weight) (Fig. 3d). In turn, an increase in skin thickness (from approx. 2.2 mm to approx. 4.2 mm, by approx. 90%) was accompanied by an increase in reducing sugar content (Fig. 3e) and L-ascorbic acid content (from approx. 98 mg∙100 g−1 fresh weight to approx. 118 mg∙100 g−1 fresh weight, by approx. 20%) (Fig. 3f). An increase in the vertical diameter of fruit from around 9.8 cm to around 16.2 cm decreased their reducing sugar content by around 50% (Fig. 3a).Figure 2Relationships between the biometric parameters and chemical composition of fruit in sweet cultivars of Capsicum annuum: (a) weight and dry matter content, (b) vertical diameter and L-ascorbic acid content, (c) horizontal diameter and dry matter content.Full size imageFigure 3Relationships between the biometric parameters and chemical composition of fruit in hot cultivars of Capsicum annuum: (a) vertical diameter and reducing sugar content, (b) horizontal diameter and total sugar content, (c) horizontal diameter and reducing sugar content, (d) horizontal diameter and nitrate (V) content, (e) skin thickness and reducing sugar content, (f) skin thickness and L-ascorbic acid content.Full size imageIn the group of the chemical composition parameters of fruit, the strongest correlation was found between total sugar content and reducing sugar content (R2 = 0.72) in sweet cultivars (Fig. 4a), and between total sugar content and nitrate (V) content (R2 = 0.59) in hot cultivars (Fig. 4b). These relationships can be described by linear functions. An increase in the total sugar content of sweet peppers from around 2.0 g∙100 g−1 fresh weight to around 5.0 g∙100 g−1 fresh weight (by approx. 150%) was accompanied by an increase in reducing sugar content by around 150%, which indicates that the ratio between both sugar fractions remained unchanged. An increase in the total sugar content of hot peppers from around 5.8 g∙100 g−1 fresh weight to around 11.1 g∙100 g−1 fresh weight (by approx. 90%) was accompanied by an increase in nitrate (V) content from around 110 mg N-NO3 kg−1 fresh weight to around 250 mg N-NO3 kg−1 fresh weight (by approx. 120%).Figure 4Relationships between the chemical composition of Capsicum annuum fruit: (a) total sugar content and reducing sugar content of sweet peppers, (b) total sugar content and nitrate (V) content of hot peppers.Full size image More

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16 November 2021

Link knowledge and action networks to tackle disasters

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Rita R. Colwell

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Charles F. Kennel

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Jim Falk

University of Melbourne, Melbourne, Australia.

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University of Maryland, College Park, USA.

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Scripps Institution of Oceanography, San Diego, USA.

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University of Arizona, Tuscon, USA.

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Earth’s climate, ecological and human systems could converge into a comprehensive crisis within our children’s lifetimes, driven by factors such as inequality, inadequate health infrastructure and food insecurity (see consensus statement, J. Falk et al. Sustain. Sci. https://doi.org/g5bd; 2021). As the COVID-19 pandemic has revealed, national military and economic security provide inadequate protection against global catastrophes.

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Nature 599, 372 (2021)
doi: https://doi.org/10.1038/d41586-021-03419-0

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