Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota
Artificial sweeteners (AS) are extensively utilized as sugar substitutes and have been recognized as emerging environmental contaminants. While the effect of AS on aquatic organisms has garnered recent attention, their effects on soil invertebrates and gut microbial communities remain unclear. To ad...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | Environment International |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412024000825 |
| _version_ | 1797248425202286592 |
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| author | Xiang-Long Lin Fei Guo Matthias C. Rillig Chun Chen Gui-Lan Duan Yong-Guan Zhu |
| author_facet | Xiang-Long Lin Fei Guo Matthias C. Rillig Chun Chen Gui-Lan Duan Yong-Guan Zhu |
| author_sort | Xiang-Long Lin |
| collection | DOAJ |
| description | Artificial sweeteners (AS) are extensively utilized as sugar substitutes and have been recognized as emerging environmental contaminants. While the effect of AS on aquatic organisms has garnered recent attention, their effects on soil invertebrates and gut microbial communities remain unclear. To address this knowledge gap, we exposed springtails (Folsomia candida) to both single and combined treatments of four typical AS (sucralose [SUC], saccharin [SAC], cyclamate [CYC], and acesulfame [ACE]) at environmentally relevant concentrations of 0.01, 0.1 and 1 mg kg−1 in soil. Following the first-generational exposure, the reproduction of juveniles showed a significant increase under all the AS treatments of 0.1 mg kg−1. The transcriptomic analysis revealed significant enrichment of several Kyoto Encyclopedia of Gene and Genome pathways (e.g., glycolysis/gluconeogenesis, pentose and glucuronate interconversions, amino sugar, and nucleotide sugar metabolism, ribosome, and lysosome) in springtails under all AS treatments. Analysis of gut bacterial microbiota indicated that three AS (SUC, CYC, and ACE) significantly decreased alpha diversity, and all AS treatments increased the abundance of the genus Achromobacter. After the sixth-generational exposure to CYC, weight increased, but reproduction was inhibited. The pathways that changed significantly (e.g., extracellular matrix-receptor interaction, amino sugar and nucleotide sugar metabolism, lysosome) were generally similar to those altered in first-generational exposure, but with opposite regulation directions. Furthermore, the effect on the alpha diversity of gut microbiota was contrary to that after first-generational exposure, and more noticeable disturbances in microbiota composition were observed. These findings underscore the ecological risk of AS in soils and improve our understanding of the toxicity effects of AS on living organisms. |
| first_indexed | 2024-03-08T00:24:01Z |
| format | Article |
| id | doaj.art-944e0c9ec08e4643b0da34f9ac2d2042 |
| institution | Directory Open Access Journal |
| issn | 0160-4120 |
| language | English |
| last_indexed | 2024-04-24T20:14:23Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Environment International |
| spelling | doaj.art-944e0c9ec08e4643b0da34f9ac2d20422024-03-23T06:22:02ZengElsevierEnvironment International0160-41202024-03-01185108496Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiotaXiang-Long Lin0Fei Guo1Matthias C. Rillig2Chun Chen3Gui-Lan Duan4Yong-Guan Zhu5State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, ChinaState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100000, ChinaInstitut Für Biologie, Freie Universität Berlin, Berlin 14195, GermanyState Key Laboratory of Crop Stress Biology for Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; University of Chinese Academy of Sciences, Beijing 100049, China; State Key Laboratory of Crop Stress Biology for Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, China; Corresponding author at: State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China.State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; University of Chinese Academy of Sciences, Beijing 100049, China; Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, ChinaArtificial sweeteners (AS) are extensively utilized as sugar substitutes and have been recognized as emerging environmental contaminants. While the effect of AS on aquatic organisms has garnered recent attention, their effects on soil invertebrates and gut microbial communities remain unclear. To address this knowledge gap, we exposed springtails (Folsomia candida) to both single and combined treatments of four typical AS (sucralose [SUC], saccharin [SAC], cyclamate [CYC], and acesulfame [ACE]) at environmentally relevant concentrations of 0.01, 0.1 and 1 mg kg−1 in soil. Following the first-generational exposure, the reproduction of juveniles showed a significant increase under all the AS treatments of 0.1 mg kg−1. The transcriptomic analysis revealed significant enrichment of several Kyoto Encyclopedia of Gene and Genome pathways (e.g., glycolysis/gluconeogenesis, pentose and glucuronate interconversions, amino sugar, and nucleotide sugar metabolism, ribosome, and lysosome) in springtails under all AS treatments. Analysis of gut bacterial microbiota indicated that three AS (SUC, CYC, and ACE) significantly decreased alpha diversity, and all AS treatments increased the abundance of the genus Achromobacter. After the sixth-generational exposure to CYC, weight increased, but reproduction was inhibited. The pathways that changed significantly (e.g., extracellular matrix-receptor interaction, amino sugar and nucleotide sugar metabolism, lysosome) were generally similar to those altered in first-generational exposure, but with opposite regulation directions. Furthermore, the effect on the alpha diversity of gut microbiota was contrary to that after first-generational exposure, and more noticeable disturbances in microbiota composition were observed. These findings underscore the ecological risk of AS in soils and improve our understanding of the toxicity effects of AS on living organisms.http://www.sciencedirect.com/science/article/pii/S0160412024000825Artificial sweetenersSoil springtailsToxicity effectsMultigenerational exposure |
| spellingShingle | Xiang-Long Lin Fei Guo Matthias C. Rillig Chun Chen Gui-Lan Duan Yong-Guan Zhu Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota Environment International Artificial sweeteners Soil springtails Toxicity effects Multigenerational exposure |
| title | Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| title_full | Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| title_fullStr | Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| title_full_unstemmed | Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| title_short | Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| title_sort | effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota |
| topic | Artificial sweeteners Soil springtails Toxicity effects Multigenerational exposure |
| url | http://www.sciencedirect.com/science/article/pii/S0160412024000825 |
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