Interactive effects of warming, antibiotics, and nanoplastics on the gut microbiome of the collembolan Folsomia candida

Highlights

	● At 20 °C antibiotic exposure led to a loss of gut microbiome evenness.
	● Gram-negative bacteria targeted by colistin were not globally affected.
	● At 20 °C nanoplastic exposure reduced relative abundance of Actinobacteria and Firmicutes .
	● Wolbachia genus controlled compositional shifts under nanoplastic addition.
	● At 22 °C nanoplastic exposure reduced abundance, increased evenness, and changed gut microbiome composition.

Abstract

Nanoplastics and antibiotics are among the most abundant chemical pollutants of soils, but their interplay with global warming remains poorly understood. The springtail Folsomia candida (Class Collembola) is a standard model for ecotoxicological assays with potential as a bioindicator ofxenobiotics. Little is known, however, about their gut microbiome and how itmight respond to warming and these pollutants. We exposed populations of F. candida to nanoplastics and antibiotic under two temperatures. The antibiotic treatment consisted of colistin addition, and the nanoplastic treatment consisted of polystyrene particles (50 mg kg^‒1 and 0.1 g kg^‒1 of dry soil, respectively). Both treatments were incubated at 20 and 22 °C for two months, and the bacterial gut microbiomes of springtails were then sequenced. Exposure to nanoplastics at 20 °C decreased the abundance of the dominant bacterial phyla and families, and decreased the evenness of the gut microbiome. At 22 °C, however, the abundances and evenness of the dominant families increased. Surprisingly, Gram-negative bacteria targeted by colistin were not globally affected. And at genus-level, the endosymbiont Wolbachia controlled the compositional shifts under nanoplastic addition, potentially driving the gut microbiome. Our results also indicated that warming was a major driver modulating the impacts of the antibiotic and nanoplastics. We illustrate how the gut microbiomes of springtails are sensitive communities responsive to xenobiotics and provide evidence of the need to combine multiple factors of global change operating simultaneously if we are to understand the responses of communities of soil arthropods and their microbiomes.

Graphical abstract

Keywords

xenobiotics / bacteria / colistin / microplastics / Folsomia candida / global change

References

[1] Agamennone, V., Jakupović, D., Weedon, J.T., Suring, W.J., van Straalen, N.M., Roelofs, D., Röling, W.F.M., 2015. The microbiome of Folsomia candida: an assessment of bacterial diversity in a Wolbachia-containing animal. FEMS Microbiology Ecology91, fiv128.

[2] Altenburger, R., Backhaus, T., Boedeker, W., Faust, M., Scholze, M., 2013. Simplifying complexity: mixture toxicity assessment in the last 20 years. Environmental Toxicology and Chemistry32, 1685–1687.

[3] Arcilla, M.S., van Hattem, J.M., Matamoros, S., Melles, D.C., Penders, J., de Jong, M.D., Schultsz, C., 2016. Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases16, 147–149.

[4] Arias-Andres, M., Klümper, U., Rojas-Jimenez, K., Grossart, H.P., 2018. Microplastic pollution increases gene exchange in aquatic ecosystems. Environmental Pollution237, 253–261.

[5] Barlaam, A., Parisi, A., Spinelli, E., Caruso, M., Taranto, P.D., Normanno, G., 2019. Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: a review. Journal of Food Protection82, 1440–1448.

[6] Beveridge, E.G., Martin, A.J., 1967. Sodium sulphomethyl derivatives of polymyxins. British Journal of Pharmacology and Chemotherapy29, 125–135.

[7] Borrelle, S.B., Ringma, J., Law, K.L., Monnahan, C.C., Lebreton, L., McGivern, A., Murphy, E., Jambeck, J., Leonard, G.H., Hilleary, M.A., Eriksen, M., Possingham, H.P., De Frond, H., Gerber, L.R., Polidoro, B., Tahir, A., Bernard, M., Mallos, N., Barnes, M., Rochman, C.M., 2020. Predicted growth in plastic waste exceeds efforts to mitigate plastic pollution. Science369, 1515–1518.

[8] Brumin, M., Kontsedalov, S., Ghanim, M., 2011. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Science18, 57–66.

[9] Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods7, 335–336.

[10] Chang, M.J., Zhang, C., Li, M.Y., Dong, J.Y., Li, C.C., Liu, J., Verheyen, J., Stoks, R., 2022. Warming, temperature fluctuations and thermal evolution change the effects of microplastics at an environmentally relevant concentration. Environmental Pollution292, 118363.

[11] Darling, E.S., Côté, I.M., 2008. Quantifying the evidence for ecological synergies. Ecology Letters11, 1278–1286.

[12] Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics26, 2460–2461.

[13] European Environment Agency, 2018. Chemicals for a sustainable future: Report of the EEA Scientific Committee Seminar : Copenhagen, 17 May 2017. Copenhagen: European Environment Agency.

[14] Feder, M.E., Hofmann, G.E., 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology61, 243–282.

[15] Fountain, M.T., Hopkin, S.P., 2005. Folsomia candida (Collembola): a “standard” soil arthropod. Annual Review of Entomology50, 201–222.

[16] Glöckner, F.O., Yilmaz, P., Quast, C., Gerken, J., Beccati, A., Ciuprina, A., Bruns, G., Yarza, P., Peplies, J., Westram, R., Ludwig, W., 2017. 25 years of serving the community with ribosomal RNA gene reference databases and tools. Journal of Biotechnology261, 169–176.

[17] Horton, A.A., Walton, A., Spurgeon, D.J., Lahive, E., Svendsen, C., 2017. Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Science of the Total Environment586, 127–141.

[18] Horváthová, T., Babik, W., Kozłowski, J., Bauchinger, U., 2019. Vanishing benefits—The loss of actinobacterial symbionts at elevated temperatures. Journal of Thermal Biology82, 222–228.

[19] Iltis, C., Tougeron, K., Hance, T., Louâpre, P., Foray, V., 2022. A perspective on insect–microbe holobionts facing thermal fluctuations in a climate-change context. Environmental Microbiology24, 18–29.

[20] Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A., Narayan, R., Law, K.L., 2015. Plastic waste inputs from land into the ocean. Science347, 768–771.

[21] Jensen, J., Krogh, P.H., Sverdrup, L.E., 2003. Effects of the antibacterial agents tiamulin, olanquindox and metronidazole and the anthelmintic ivermectin on the soil invertebrate species Folsomia fimetaria (Collembola) and Enchytraeus crypticus (Enchytraeidae). Chemosphere50, 437–443.

[22] Ji, Z.Y., Huang, Y., Feng, Y., Johansen, A., Xue, J.M., Tremblay, L.A., Li, Z.J., 2021. Effects of pristine microplastics and nanoplastics on soil invertebrates: A systematic review and meta-analysis of available data. Science of the Total Environment788, 147784.

[23] Katz, E., Demain, A.L., 1977. The peptide antibiotics of bacillus: chemistry, biogenesis, and possible functions. Bacteriological Reviews41, 449–474.

[24] Kõljalg, U., Nilsson, R.H., Abarenkov, K., Tedersoo, L., Taylor, A.F. S., Bahram, M., Bates, S.T., Bruns, T.D., Bengtsson-Palme, J., Callaghan, T.M., Douglas, B., Drenkhan, T., Eberhardt, U., Dueñas, M., Grebenc, T., Griffith, G.W., Hartmann, M., Kirk, P.M., Kohout, P., Larsson, E., Lindahl, B.D., Lücking, R., Martín, M.P., Matheny, P.B., Nguyen, N.H., Niskanen, T., Oja, J., Peay, K.G., Peintner, U., Peterson, M., Põldmaa, K., Saag, L., Saar, I., Schüßler, A., Scott, J.A., Senés, C., Smith, M.E., Suija, A., Taylor, D.L., Telleria, M.T., Weiss, M., Larsson, K.H., 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology22, 5271–5277.

[25] Law, K.L., Thompson, R.C., 2014. Microplastics in the seas. Science345, 144–145.

[26] Li, S.M., Li, J., Li, Z., Ke, X., Wu, L.H., Christie, P., 2021. Toxic effects of norfloxacin in soil on fed and unfed Folsomia candida (Isotomidae: Collembola) and on gut and soil microbiota. Science of the Total Environment788, 147793.

[27] Li, Z.X., Sun, A.Q., Liu, X.F., Chen, Q.L., Bi, L., Ren, P.X., Shen, J.P., Jin, S.S., He, J.Z., Hu, H.W., Yang, Y.S., 2022. Climate warming increases the proportions of specific antibiotic resistance genes in natural soil ecosystems. Journal of Hazardous Materials430, 128442.

[28] Liebezeit, G., Liebezeit, E., 2013. Non-pollen particulates in honey and sugar. Food Additives & Contaminants: Part A30, 2136–2140.

[29] Louca, S., Parfrey, L.W., Doebeli, M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277.

[30] Lyu, K., Cao, C., Li, D., Akbar, S., Yang, Z., 2021. The thermal regime modifies the response of aquatic keystone species Daphnia to microplastics: evidence from population fitness, accumulation, histopathological analysis and candidate gene expression. Science of the Total Environment783, 147154.

[31] MacFadden, D.R., McGough, S.F., Fisman, D., Santillana, M., Brownstein, J.S., 2018. Antibiotic resistance increases with local temperature. Nature Climate Change8, 510–514.

[32] Margulis, L., Fester, R., eds. 1991. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. Cambridge: MIT Press.

[33] McGough, S.F., MacFadden, D.R., Hattab, M.W., Mølbak, K., Santillana, M., 2020. Rates of increase of antibiotic resistance and ambient temperature in Europe: a cross-national analysis of 28 countries between 2000 and 2016. Eurosurveillance25, 4.

[34] Moe, S.J., De Schamphelaere, K., Clements, W.H., Sorensen, M.T., Van Den Brink, P.J., Liess, M., 2013. Combined and interactive effects of global climate change and toxicants on populations and communities. Environmental Toxicology and Chemistry32, 49–61.

[35] Moghadam, N.N., Thorshauge, P.M., Kristensen, T.N., de Jonge, N., Bahrndorff, S., Kjeldal, H., Nielsen, J.L., 2018. Strong responses of Drosophila melanogaster microbiota to developmental temperature. Fly12, 1–12.

[36] Ng, E.L., Lwanga, E.H., Eldridge, S.M., Johnston, P., Hu, H.W., Geissen, V., Chen, D.L., 2018. An overview of microplastic and nanoplastic pollution in agroecosystems. Science of the Total Environment627, 1377–1388.

[37] Nizzetto, L., Futter, M., Langaas, S., 2016. Are agricultural soils dumps for microplastics of urban origin. Environmental Science & Technology50, 10777–10779.

[38] Paine, R.T., Tegner, M.J., Johnson, E.A., 1998. Compounded perturbations yield ecological surprises. Ecosystems1, 535–545.

[39] Parthasarathy, A., Tyler, A.C., Hoffman, M.J., Savka, M.A., Hudson, A.O., 2019. Is plastic pollution in aquatic and terrestrial environments a driver for the transmission of pathogens and the evolution of antibiotic resistance. Environmental Science & Technology53, 1744–1745.

[40] Persson, L., Carney Almroth, B.M., Collins, C.D., Cornell, S., de Wit, C.A., Diamond, M.L., Fantke, P., Hassellöv, M., MacLeod, M., Ryberg, M.W., Søgaard Jørgensen, P., Villarrubia-Gómez, P., Wang, Z.Y., Hauschild, M.Z., 2022. Outside the safe operating space of the planetary boundary for novel entities. Environmental Science & Technology56, 1510–1521.

[41] Pike, N., Kingcombe, R., 2009. Antibiotic treatment leads to the elimination of Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia candida. BMC Biology7, 54.

[42] Qi, R.M., Jones, D.L., Li, Z., Liu, Q., Yan, C.R., 2020. Behavior of microplastics and plastic film residues in the soil environment: A critical review. Science of the Total Environment703, 134722.

[43] R Core Team, 2020. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

[44] Rhouma, M., Madec, J.Y., Laxminarayan, R., 2023. Colistin: from the shadows to a one health approach for addressing antimicrobial resistance. International Journal of Antimicrobial Agents61, 106713.

[45] Rillig, M.C., 2012. Microplastic in terrestrial ecosystems and the soil. Environmental Science & Technology46, 6453–6454.

[46] Rillig, M.C., de Souza Machado, A.A., Lehmann, A., Klümper, U., 2019a. Evolutionary implications of microplastics for soil biota. Environmental Chemistry16, 3–7.

[47] Rillig, M.C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C.A., Buchert, S., Wulf, A., Iwasaki, A., Roy, J., Yang, G.W., 2019b. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science366, 886–890.

[48] Rockström, J., Steffen, W., Noone, K., Persson, Å., Chapin III, F.S., Lambin, E., Lenton, T.M., Scheffer, M., Folke, C., Schellnhuber, H.J., Nykvist, B., de Wit, C.A., Hughes, T., van der Leeuw, S., Rodhe, H., Sörlin, S., Snyder, P.K., Costanza, R., Svedin, U., Falkenmark, M., Karlberg, L., Corell, R.W., Fabry, VJ.., Hansen, J., Walker, B., Liverman, D., Richardson, K., Crutzen, P., Foley, J., 2009. Planetary boundaries: exploring the safe operating space for humanity. Ecology and Society14, 32.

[49] Shen, M.C., Zhang, Y.X., Zhu, Y., Song, B., Zeng, G.M., Hu, D.F., Wen, X.F., Ren, X.Y., 2019. Recent advances in toxicological research of nanoplastics in the environment: a review. Environmental Pollution252, 511–521.

[50] Sigmund, G., Ågerstrand, M., Antonelli, A., Backhaus, T., Brodin, T., Diamond, M.L., Erdelen, W.R., Evers, D.C., Hofmann, T., Hueffer, T., Lai, A., Torres, J.P.M., Mueller, L., Perrigo, A.L., Rillig, M.C., Schaeffer, A., Scheringer, M., Schirmer, K., Tlili, A., Soehl, A., Triebskorn, R., Vlahos, P., Vom Berg, C., Wang, Z.Y., Groh, K.J., 2023. Addressing chemical pollution in biodiversity research. Global Change Biology29, 3240–3255.

[51] Steffen, W., Richardson, K., Rockström, J., Cornell, S.E., Fetzer, I., Bennett, E.M., Biggs, R., Carpenter, S.R., de Vries, W., de Wit, C.A., Folke, C., Gerten, D., Heinke, J., Mace, G.M., Persson, L.M., Ramanathan, V., Reyers, B., Sörlin, S., 2015. Planetary boundaries: guiding human development on a changing planet. Science347, 1259855.

[52] Thimm, T., Hoffmann, A., Borkott, H., Charles Munch, J., Tebbe, C.C., 1998. The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Applied and Environmental Microbiology64, 2660–2669.

[53] Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G., McGonigle, D., Russell, A.E., 2012. Lost at sea: where is all the plastic. Science304, 838–838.

[54] Wang, C.C., Feng, Y., Liu, L.N., Wei, L., Kang, M., Zong, Z.Y., 2020. Identification of novel mobile colistin resistance gene mcr-10. Emerging Microbes & Infections9, 508–516.

[55] Warton, D.I., Wright, S.T., Wang, Y., 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution3, 89–101.

[56] Wiesner, M.R., Lowry, G.V., Casman, E., Bertsch, P.M., Matson, C.W., Di Giulio, R.T., Liu, J., Hochella, M.F., 2011. Meditations on the ubiquity and mutability of nano-sized materials in the environment. ACS Nano5, 8466–8470.

[57] Wypych, T.P., Marsland, B.J., 2018. Antibiotics as instigators of microbial dysbiosis: implications for asthma and allergy. Trends in Immunology39, 697–711.

[58] Xi, Z.Y., Gavotte, L., Xie, Y., Dobson, S.L., 2008. Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host. BMC Genomics9, 1.

[59] Xiang, Q., Zhu, D., Chen, Q.L., Delgado-Baquerizo, M., Su, J.Q., Qiao, M., Yang, X.R., Zhu, Y.G., 2019. Effects of diet on gut microbiota of soil collembolans. Science of the Total Environment676, 197–205.

[60] Zhang, C., Song, Z.L., Zhuang, D.H., Wang, J., Xie, S.S., Liu, G.B., 2019a. Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biology and Fertility of Soils55, 229–242.

[61] Zhang, Q., Zhu, D., Ding, J., Zhou, S.Y.D., Sun, L.W., Qian, H.F., 2019b. Species-specific response of the soil collembolan gut microbiome and resistome to soil oxytetracycline pollution. Science of the Total Environment668, 1183–1190.

[62] Zhu, D., An, X.L., Chen, Q.L., Yang, X.R., Christie, P., Ke, X., Wu, L.H., Zhu, Y.G., 2018a. Antibiotics disturb the microbiome and increase the incidence of resistance genes in the gut of a common soil collembolan. Environmental Science & Technology52, 3081–3090.

[63] Zhu, D., Chen, Q.L., An, X.L., Yang, X.R., Christie, P., Ke, X., Wu, L.H., Zhu, Y.G., 2018b. Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition. Soil Biology and Biochemistry116, 302–310.

[64] Zortéa, T., Segat, J.C., Maccari, A.P., Sousa, J.P., Da Silva, A.S., Baretta, D., 2017. Toxicity of four veterinary pharmaceuticals on the survival and reproduction of Folsomia candida in tropical soils. Chemosphere173, 460–465.

Acknowledgements

This work was supported by the Spanish Government grants PID2020115770RB-I, TED2021-132627 B–I00 and PID2022-140808NB-I00; funded by MCIN; AEI/10.13039/501100011033 European Union Next Generation EU/PRTR; the Fundación Ramón Areces grant CIVP20A6621; and the Catalan Government grant SGR 2021–1333.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0269-8 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2024 Higher Education Press