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Metabolomics for early detection of stress in freshwater alga Poterioochromonas malhamensis exposed to silver nanoparticles.

ABSTRACT: Silver nanoparticles (AgNPs) are one of the most used engineered nanomaterials. Despite progress in assessing their environmental implications, knowledge gaps exist concerning the metabolic perturbations induced by AgNPs on phytoplankton, essential organisms in global biogeochemical cycles and food-web dynamics. We combine targeted metabolomics, biouptake and physiological response studies to elucidate metabolic perturbations in alga Poterioochromonas malhamensis induced by AgNPs and dissolved Ag. We show time-dependent perturbation of the metabolism of amino acids, nucleotides, fatty acids, tricarboxylic acids, photosynthesis and photorespiration by both Ag-treatments. The results suggest that dissolved Ag ions released by AgNPs are the major toxicity driver; however, AgNPs internalized in food vacuoles contributed to the perturbation of amino acid metabolism, TCA cycle and oxidative stress. The metabolic perturbations corroborate the observed physiological responses. We highlight the potential of metabolomics as a tool for understanding the molecular basis for these metabolic and physiological changes, and for early detection of stress.

SUBMITTER: Liu W

PROVIDER: S-EPMC7689461 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Metabolomics for early detection of stress in freshwater alga Poterioochromonas malhamensis exposed to silver nanoparticles.

Liu Wei W Majumdar Sanghamitra S Majumdar Sanghamitra S Li Weiwei W Keller Arturo A AA Slaveykova Vera I VI

Scientific reports 20201125 1

Silver nanoparticles (AgNPs) are one of the most used engineered nanomaterials. Despite progress in assessing their environmental implications, knowledge gaps exist concerning the metabolic perturbations induced by AgNPs on phytoplankton, essential organisms in global biogeochemical cycles and food-web dynamics. We combine targeted metabolomics, biouptake and physiological response studies to elucidate metabolic perturbations in alga Poterioochromonas malhamensis induced by AgNPs and dissolved A ...[more]

PMID: 33239722

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Project description:Aquatic environments are heavily impacted by human activities including climate warming and the introduction of xenobiotics. Due to the application of silver nanoparticles as bactericidal agent the introduction of silver into the environment strongly has increased during the past years. Silver ions affect the primary metabolism of algae, in particular photosynthesis. Mixotrophic algae are an interesting test case as they do not exclusively rely on photosynthesis which may attenuate the harmful effect of silver. In order to study the effect of silver ions on mixotrophs, cultures of the chrysophyte Poterioochromonas malhamensis were treated in a replicate design in light and darkness with silver nitrate at a sub-lethal concentration. At five time points samples were taken for the identification and quantitation of proteins by mass spectrometry. In our analysis, relative quantitative protein mass spectrometry has shown to be a useful tool for functional analyses in conjunction with transcriptome reference sequences. A total of 3,952 proteins in 63 samples were identified and quantified, mapping to 4,829 transcripts of the sequenced and assembled transcriptome. Among them, 720 and 104 proteins performing various cellular functions were differentially expressed after eight days in light versus darkness and after three days of silver treatment, respectively. Specifically pathways of the energy and primary carbon metabolism were differentially affected by light and the utilization of expensive reactions hints to an energy surplus of P. malhamensis under light conditions. The excess energy is not invested in growth, but in the synthesis of storage metabolites. The effects of silver were less explicit, observable especially in the dark treatments where the light effect could not mask coinciding but weaker effects of silver. Photosynthesis, particularly the light harvesting complexes, and several sulphur containing enzymes were affected presumably due to a direct interference with the silver ions, mainly affecting energy supply.

Project description:Mixotrophic flagellates, which have diverse nutritional modes and play important roles in connecting the microbial loop with the classical food chain, are ideal models to study the mechanisms of adaptation between different nutritional modes in protists. In their natural ecosystems, mixotrophic flagellates may encounter microalgal prey of different digestibility, which may affect the carbon flow. To date, a molecular biological view of the metabolic processes in the mixotrophic flagellate Poterioochromonas malhamensis during nutritional adaptation and feeding on microalgal prey of different digestibility is still lacking. Accordingly, this study focused on the gene expression differences in P. malhamensis under autotrophy, being fed by the digestible microalga Chlorella sorokiniana GT-1, and being fed by the indigestible microalga C. sorokiniana CMBB-146. Results showed that the growth rate of P. malhamensis under autotrophy was much lower than that when fed by digestible microalgae. Addition of C. sorokiniana CMBB-146 could only increase the growth rate of P. malhamensis in the first 3 days, but the cell concentration of P. malhamensis started to decrease gradually after 4 days. Compared to autotrophic P. malhamensis, total 6,583 and 3,510 genes were significantly and differentially expressed in P. malhamensis fed by digestible microalgae and indigestible microalgae, respectively. Compared to autotrophic cells, genes related to the ribosome, lysosome, glycolysis, gluconeogenesis, TCA cycle, β-oxidation, duplication, and β-1,3-glucan in P. malhamensis grazing on digestible prey were up-regulated, while genes related to light harvesting and key enzymes referring to chlorophyll were down-regulated. Genes related to apoptosis and necrosis in P. malhamensis were up-regulated after grazing on indigestible microalgae compared to the autotrophic group, which we suggest is associated with the up-regulation of genes related to lysosome enzymes. This study provides abundant information on the potential intracellular physiological responses of P. malhamensis during the process of nutritional adaptation.

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Metabolomics for early detection of stress in freshwater alga Poterioochromonas malhamensis exposed to silver nanoparticles.

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Metabolomics for early detection of stress in freshwater alga Poterioochromonas malhamensis exposed to silver nanoparticles.

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