Tolerance to environmental pollution in the freshwater crustacean Asellus aquaticus: A role for the microbiome

. 2024 Jun ; 16 (3) : e13252.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38783543

Grantová podpora
DUE-Mobil Grant from the University of Duisburg-Essen
CZ.02.2.69/0.0/0.0/20_079/0017809 Ministry of Education, Youth and Sports of the Czech Republic
5221.00979.008.08 Eawag Academic Transition Grant
Individual Travel Grant from the Radboud University Nijmegen

Freshwater habitats are frequently contaminated by diverse chemicals of anthropogenic origin, collectively referred to as micropollutants, that can have detrimental effects on aquatic life. The animals' tolerance to micropollutants may be mediated by their microbiome. If polluted aquatic environments select for contaminant-degrading microbes, the acquisition of such microbes by the host may increase its tolerance to pollution. Here we tested for the potential effects of the host microbiome on the growth and survival of juvenile Asellus aquaticus, a widespread freshwater crustacean. Using faecal microbiome transplants, we provided newly hatched juveniles with the microbiome isolated from donor adults reared in either clean or micropollutant-contaminated water and, after transplantation, recipient juveniles were reared in water with and without micropollutants. The experiment revealed a significant negative effect of the micropollutants on the survival of juvenile isopods regardless of the received faecal microbiome. The micropollutants had altered the composition of the bacterial component of the donors' microbiome, which in turn influenced the microbiome of juvenile recipients. Hence, we show that relatively high environmental concentrations of micropollutants reduce survival and alter the microbiome composition of juvenile A. aquaticus, but we have no evidence that tolerance to micropollutants is modulated by their microbiome.

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Amoatey, P. & Baawain, M.S. (2019) Effects of pollution on freshwater aquatic organisms. Water Environment Research: A Research Publication of the Water Environment Federation, 91, 1272–1287. PubMed

Azad, M. (2013) Why are early life stages of aquatic organisms more sensitive to toxicants than adults? In: Sivakumar, G. (Ed.) New insights into toxicity and drug testing. Rijeka: IntechOpen.

Baldassarre, L. , Ying, H. , Reitzel, A.M. , Franzenburg, S. & Fraune, S. (2022) Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis . Nature Communications, 13, 3804. PubMed PMC

Bang, C. , Dagan, T. , Deines, P. , Dubilier, N. , Duschl, W.J. , Fraune, S. et al. (2018) Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology, 127, 1–19. PubMed

Bates, D. , Mächler, M. , Bolker, B. & Walker, S. (2015) Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67, 1–48.

Bayona, Y. , Roucaute, M. , Cailleaud, K. , Lagadic, L. , Bassères, A. & Caquet, T. (2015) Effect of thiram and of a hydrocarbon mixture on freshwater macroinvertebrate communities in outdoor stream and pond mesocosms: I. Study design, chemicals fate and structural responses. Ecotoxicology, 24, 1976–1995. PubMed

Bisschop, K. , Kortenbosch, H.H. , van Eldijk, T.J.B. , Mallon, C.A. , Salles, J.F. , Bonte, D. et al. (2022) Microbiome heritability and its role in adaptation of hosts to novel resources. Frontiers in Microbiology, 13, 703183. PubMed PMC

Bloor, M.C. (2011) Dietary preference of Gammarus pulex and Asellus aquaticus during a laboratory breeding programme for ecotoxicological studies. International Journal of Zoology, 2011, 294394.

Bouchon, D. , Rigaud, T. & Juchault, P. (1998) Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proceedings of the Biological Sciences, 265, 1081–1090. PubMed PMC

Bredon, M. , Herran, B. , Bertaux, J. , Grève, P. , Moumen, B. & Bouchon, D. (2020) Isopod holobionts as promising models for lignocellulose degradation. Biotechnology for Biofuels, 13, 49. PubMed PMC

Bredon, M. , Herran, B. , Lheraud, B. , Bertaux, J. , Grève, P. , Moumen, B. et al. (2019) Lignocellulose degradation in isopods: new insights into the adaptation to terrestrial life. BMC Genomics, 20, 462. PubMed PMC

Bruijning, M. , Henry, L.P. , Forsberg, S.K.G. , Metcalf, C.J.E. & Ayroles, J.F. (2022) Natural selection for imprecise vertical transmission in host–microbiota systems. Nature Ecology & Evolution, 6, 77–87. PubMed PMC

Bulteel, L. , Houwenhuyse, S. , Declerck, S.A.J. & Decaestecker, E. (2021) The role of microbiome and genotype in Daphnia magna upon parasite re‐exposure. Genes, 12, 70. PubMed PMC

Bundschuh, M. , Appeltauer, A. , Dabrunz, A. & Schulz, R. (2012) Combined effect of invertebrate predation and sublethal pesticide exposure on the behavior and survival of Asellus aquaticus (Crustacea; Isopoda). Archives of Environmental Contamination and Toxicology, 63, 77–85. PubMed

Callens, M. , De Meester, L. , Muylaert, K. , Mukherjee, S. & Decaestecker, E. (2020) The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community. FEMS Microbiology Ecology, 96, fiaa128. PubMed PMC

Ciślak, M. , Kruszelnicka, I. , Zembrzuska, J. & Ginter‐Kramarczyk, D. (2023) Estrogen pollution of the European aquatic environment: a critical review. Water Research, 229, 119413. PubMed

Claus, S.P. , Guillou, H. & Ellero‐Simatos, S. (2016) The gut microbiota: a major player in the toxicity of environmental pollutants? npj Biofilms and Microbiomes, 2, 16003. PubMed PMC

Coon, K.L. , Hegde, S. & Hughes, G.L. (2022) Interspecies microbiome transplantation recapitulates microbial acquisition in mosquitoes. Microbiome, 10, 58. PubMed PMC

De Lange, H.J. , Sperber, V. & Peeters, E.T.H.M. (2006) Avoidance of polycyclic aromatic hydrocarbon–contaminated sediments by the freshwater invertebrates Gammarus pulex and Asellus aquaticus . Environmental Toxicology and Chemistry, 25, 452–457. PubMed

de Nicola, G.M. , Migliore, L. & Guarino, S.M. (1987) Sensitivity of Asellus aquaticus (L.) and Proasellus coxalis Dollf. (Crustacea, Isopoda) to copper. Hydrobiologia, 146, 63–69.

Debray, R. , Herbert, R.A. , Jaffe, A.L. , Crits‐Christoph, A. , Power, M.E. & Koskella, B. (2022) Priority effects in microbiome assembly. Nature Reviews Microbiology, 20, 109–121. PubMed

Decaestecker, E. , Van de Moortel, B. , Mukherjee, S. , Gurung, A. , Stoks, R. & De Meester, L. (2024) Hierarchical eco‐evo dynamics mediated by the gut microbiome. Trends in Ecology & Evolution, 39, 165–174. PubMed

DeFur, P.L. (2004) Use and role of invertebrate models in endocrine disruptor research and testing. ILAR Journal, 45, 484–493. PubMed

Delhoumi, M. , Catania, V. , Zaabar, W. , Tolone, M. , Quatrini, P. & Achouri, M.S. (2020) The gut microbiota structure of the terrestrial isopod Porcellionides pruinosus (Isopoda: Oniscidea). The European Zoological Journal, 87, 357–368.

Dhariwal, A. , Chong, J. , Habib, S. , King, I.L. , Agellon, L.B. & Xia, J. (2017) MicrobiomeAnalyst: a web‐based tool for comprehensive statistical, visual and meta‐analysis of microbiome data. Nucleic Acids Research, 45, W180–W188. PubMed PMC

Díaz, S. , Escobar, J.S. & Avila, F.W. (2021) Identification and removal of potential contaminants in 16S rRNA gene sequence data sets from low‐microbial‐biomass samples: an example from mosquito tissues. mSphere, 6, e0050621. PubMed PMC

Dittmer, J. , Lesobre, J. , Moumen, B. & Bouchon, D. (2016) Host origin and tissue microhabitat shaping the microbiota of the terrestrial isopod Armadillidium vulgare . FEMS Microbiology Ecology, 92, fiw063. PubMed

Drew, G.C. , Stevens, E.J. & King, K.C. (2021) Microbial evolution and transitions along the parasite–mutualist continuum. Nature Reviews Microbiology, 19, 623–638. PubMed PMC

Eckert, E.M. , Amalfitano, S. , Di Cesare, A. , Manzari, C. , Corno, G. & Fontaneto, D. (2020) Different substrates within a lake harbour connected but specialised microbial communities. Hydrobiologia, 847, 1689–1704.

Eisenhofer, R. , Minich, J.J. , Marotz, C. , Cooper, A. , Knight, R. & Weyrich, L.S. (2019) Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends in Microbiology, 27, 105–117. PubMed

Engel, P. & Moran, N.A. (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiology Reviews, 37, 699–735. PubMed

Fleeger, J.W. , Carman, K.R. & Nisbet, R.M. (2003) Indirect effects of contaminants in aquatic ecosystems. Science of the Total Environment, 317, 207–233. PubMed

Fraser, J. (1980) Acclimation to lead in the freshwater isopod Asellus aquaticus . Oecologia, 45, 419–420. PubMed

Gardeström, J. , Ermold, M. , Goedkoop, W. & McKie, B.G. (2016) Disturbance history influences stressor impacts: effects of a fungicide and nutrients on microbial diversity and litter decomposition. Freshwater Biology, 61, 2171–2184.

Gilbert, S.F. , Sapp, J. & Tauber, A.I. (2012) A symbiotic view of life: we have never been individuals. The Quarterly Review of Biology, 87, 325–341. PubMed

González, R. & Elena, S.F. (2021) The interplay between the host microbiome and pathogenic viral infections. MBio, 12, e0249621. PubMed PMC

Goodyear, K.L. & McNeill, S. (1999) Bioaccumulation of heavy metals by aquatic macro‐invertebrates of different feeding guilds: a review. Science of the Total Environment, 229, 1–19.

Graça, M.A.S. , Maltby, L. & Calow, P. (1993) Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus. II. Effects on growth, reproduction and physiology. Oecologia, 96, 304–309. PubMed

Graça, M.A.S. , Maltby, L. & Calow, P. (1994) Comparative ecology of Gammarus pulex (L.) and Asellus aquaticus (L.) I: population dynamics and microdistribution. Hydrobiologia, 281, 155–162.

Grieneisen, L. , Dasari, M. , Gould, T.J. , Björk, J.R. , Grenier, J.C. , Yotova, V. et al. (2021) Gut microbiome heritability is nearly universal but environmentally contingent. Science (New York, N.Y.), 373, 181–186. PubMed PMC

Griffiths, S.M. , Antwis, R.E. , Lenzi, L. , Lucaci, A. , Behringer, D.C. , Butler, M.J. et al. (2019) Host genetics and geography influence microbiome composition in the sponge Ircinia campana . The Journal of Animal Ecology, 88, 1684–1695. PubMed PMC

Guo, W. , Ren, K. , Ning, R. , Li, C. , Zhang, H. , Li, D. et al. (2020) Fecal microbiota transplantation provides new insight into wildlife conservation. Global Ecology and Conservation, 24, e01234.

Halstead, N.T. , McMahon, T.A. , Johnson, S.A. , Raffel, T.R. , Romansic, J.M. , Crumrine, P.W. et al. (2014) Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecology Letters, 17, 932–941. PubMed

Hammer, T.J. , Dickerson, J.C. & Fierer, N. (2015) Evidence‐based recommendations on storing and handling specimens for analyses of insect microbiota. PeerJ, 3, e1190. PubMed PMC

Hector, K.L. & Nakagawa, S. (2012) Quantitative analysis of compensatory and catch‐up growth in diverse taxa. Journal of Animal Ecology, 81, 583–593. PubMed

Henry, L.P. , Bruijning, M. , Forsberg, S.K.G. & Ayroles, J.F. (2021) The microbiome extends host evolutionary potential. Nature Communications, 12, 5141. PubMed PMC

Hernandez, D.J. , David, A.S. , Menges, E.S. , Searcy, C.A. & Afkhami, M.E. (2021) Environmental stress destabilizes microbial networks. The ISME Journal, 15, 1722–1734. PubMed PMC

Holt, C.C. , van der Giezen, M. , Daniels, C.L. , Stentiford, G.D. & Bass, D. (2020) Spatial and temporal axes impact ecology of the gut microbiome in juvenile European lobster (Homarus gammarus). The ISME Journal, 14, 531–543. PubMed PMC

Hornung, B.V.H. , Zwittink, R.D. & Kuijper, E.J. (2019) Issues and current standards of controls in microbiome research. FEMS Microbiology Ecology, 95, fiz045. PubMed PMC

Horvathova, T. , Babik, W. & Bauchinger, U. (2016) Biofilm feeding: microbial colonization of food promotes the growth of a detritivorous arthropod. ZooKeys, 577, 25–41. PubMed PMC

Horváthová, T. , Babik, W. , Kozłowski, J. & Bauchinger, U. (2019) Vanishing benefits—the loss of actinobacterial symbionts at elevated temperatures. Journal of Thermal Biology, 82, 222–228. PubMed

Hsu, B.‐Y. , Dijkstra, C. & Groothuis, T.G.G. (2017) Organizing effects of adverse early‐life condition on body mass, compensatory growth and reproduction: experimental studies in rock pigeons. Journal of Avian Biology, 48, 1166–1176.

Huey, R.B. , Kearney, M.R. , Krockenberger, A. , Holtum, J.A.M. , Jess, M. & Williams, S.E. (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society, B: Biological Sciences, 367, 1665–1679. PubMed PMC

Hutchinson, T.H. , Solbe, J. & Kloepper‐Sams, P.J. (1998) Analysis of the ecetoc aquatic toxicity (EAT) database III—comparative toxicity of chemical substances to different life stages of aquatic organisms. Chemosphere, 36, 129–142.

Huus, K.E. & Ley, R.E. (2021) Blowing hot and cold: body temperature and the microbiome. mSystems, 6, e0070721. Available from: 10.1128/msystems.00707-00721 PubMed DOI PMC

Ieromina, O. , Peijnenburg, W.J.G.M. , de Snoo, G.R. & Vijver, M.G. (2014) Population responses of Daphnia magna, Chydorus sphaericus and Asellus aquaticus in pesticide contaminated ditches around bulb fields. Environmental Pollution, 192, 196–203. PubMed

Ihnen, K. & Zimmer, M. (2008) Selective consumption and digestion of litter microbes by Porcellio scaber (Isopoda: Oniscidea). Pedobiologia, 51, 335–342.

Itoh, H. , Tago, K. , Hayatsu, M. & Kikuchi, Y. (2018) Detoxifying symbiosis: microbe‐mediated detoxification of phytotoxins and pesticides in insects. Natural Product Reports, 35, 434–454. PubMed

Kassambara, A. , Kosinski, M. & Biecek, P. (2020) Drawing survival curves using ‘ggplot2’.2020. https://rpkgsdatanoviacom/survminer/indexhtml

Kikuchi, Y. , Hayatsu, M. , Hosokawa, T. , Nagayama, A. , Tago, K. & Fukatsu, T. (2012) Symbiont‐mediated insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America, 109, 8618–8622. PubMed PMC

Kim, P.S. , Shin, N.‐R. , Lee, J.‐B. , Kim, M.‐S. , Whon, T.W. , Hyun, D.‐W. et al. (2021) Host habitat is the major determinant of the gut microbiome of fish. Microbiome, 9, 166. PubMed PMC

Knigge, T. , LeBlanc, G.A. & Ford, A.T. (2021) A crab is not a fish: unique aspects of the crustacean endocrine system and considerations for endocrine toxicology. Frontiers in Endocrinology, 12, 587608. PubMed PMC

Koliada, A. , Moseiko, V. , Romanenko, M. , Piven, L. , Lushchak, O. , Kryzhanovska, N. et al. (2020) Seasonal variation in gut microbiota composition: cross‐sectional evidence from Ukrainian population. BMC Microbiology, 20, 100. PubMed PMC

Kolodny, O. & Schulenburg, H. (2020) Microbiome‐mediated plasticity directs host evolution along several distinct time scales. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 375, 20190589. PubMed PMC

Könemann, S. , Müller, Y. , Tschentscher, D. , Krauss, M. , Inostroza, P.A. , Brückner, I. et al. (2019) Combination of in situ feeding rate experiments and chemical body burden analysis to assess the influence of micropollutants in wastewater on Gammarus pulex . International Journal of Environmental Research and Public Health, 16, 883–896. PubMed PMC

Kuznetsova, A. , Brockhoff, P.B. , Christensen, R.H. , Brockhoff, P.B. , Christensen, R.H.B. , Kuznetsova, T.A. et al. (2014) lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package).

Lafuente, E. , Carles, L. , Walser, J.C. , Giulio, M. , Wullschleger, S. , Stamm, C. et al. (2023) Effects of anthropogenic stress on hosts and their microbiomes: treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus). Evolutionary Applications, 16, 824–848. PubMed PMC

Lafuente, E. , Lürig, M.D. , Rövekamp, M. , Matthews, B. , Buser, C. , Vorburger, C. et al. (2021) Building on 150 years of knowledge: the freshwater isopod Asellus aquaticus as an integrative eco‐evolutionary model system. Frontiers in Ecology and Evolution, 9, 748212.

Lagadic, L. & Caquet, T. (1998) Invertebrates in testing of environmental chemicals: are they alternatives? Environmental Health Perspectives, 106(Suppl 2), 593–611. PubMed PMC

Lahti, L. & Shetty, S. (2018) Introduction to the microbiome R package. https://microbiomegithubio/tutorials

Landrigan, P.J. , Stegeman, J.J. , Fleming, L.E. , Allemand, D. , Anderson, D.M. , Backer, L.C. et al. (2020) Human health and ocean pollution. Annals of Global Health, 86, 151. PubMed PMC

Lavrinienko, A. , Tukalenko, E. , Mappes, T. & Watts, P.C. (2018) Skin and gut microbiomes of a wild mammal respond to different environmental cues. Microbiome, 6, 209. PubMed PMC

Legan, T.B. , Lavoie, B. & Mawe, G.M. (2022) Direct and indirect mechanisms by which the gut microbiota influence host serotonin systems. Neurogastroenterology and Motility, 34, e14346. PubMed PMC

Li, J. , Bates, K.A. , Hoang, K.L. , Hector, T.E. , Knowles, S.C.L. & King, K.C. (2023) Experimental temperatures shape host microbiome diversity and composition. Global Change Biology, 29, 41–56. PubMed PMC

Liao, A. , Hartikainen, H. & Buser, C.C. (2023) Individual level microbial communities in the digestive system of the freshwater isopod Asellus aquaticus: complex, robust and prospective. Environmental Microbiology Reports, 15, 188–196. PubMed PMC

Love, M.I. , Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biology, 15, 550. PubMed PMC

Macke, E. , Callens, M. , De Meester, L. & Decaestecker, E. (2017) Host‐genotype dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nature Communications, 8, 1608. PubMed PMC

Malaj, E. , von der Ohe, P.C. , Grote, M. , Kühne, R. , Mondy, C.P. , Usseglio‐Polatera, P. et al. (2014) Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. Proceedings of the National Academy of Sciences, 111, 9549–9554. PubMed PMC

Maltby, L. (1991) Pollution as a probe of life‐history adaptation in Asellus aquaticus (Isopoda). Oikos, 61, 11–18.

Martiny, J.B.H. , Martiny, A.C. , Brodie, E. , Chase, A.B. , Rodríguez‐Verdugo, A. , Treseder, K.K. et al. (2023) Investigating the eco‐evolutionary response of microbiomes to environmental change. Ecology Letters, 00, 1–10. PubMed

McFall‐Ngai, M. , Hadfield, M.G. , Bosch, T.C.G. , Carey, H.V. , Domazet‐Lošo, T. , Douglas, A.E. et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences, 110, 3229–3236. PubMed PMC

McMurdie, P.J. & Holmes, S. (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, e61217. PubMed PMC

Munz, N.A. , Burdon, F.J. , de Zwart, D. , Junghans, M. , Melo, L. , Reyes, M. et al. (2017) Pesticides drive risk of micropollutants in wastewater‐impacted streams during low flow conditions. Water Research, 110, 366–377. PubMed

Naylor, C. , Pindar, L. & Calow, P. (1990) Inter‐ and intraspecific variation in sensitivity to toxins; the effects of acidity and zinc on the freshwater crustaceans Asellus Aquaticus (L.) and Gammarus pulex (L.). Water Research, 24, 757–762.

Nussey, D.H. , Wilson, A.J. & Brommer, J.E. (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology, 20, 831–844. PubMed

O'Callaghan, I. , Harrison, S. , Fitzpatrick, D. & Sullivan, T. (2019) The freshwater isopod Asellus aquaticus as a model biomonitor of environmental pollution: a review. Chemosphere, 235, 498–509. PubMed

Oksanen, J. , Blanchet, F. , Kindt, R. , Legendre, P. , Minchin, P. , O'hara, R. et al. (2015) Vegan: community ecology package. R package vegan, vers. 2.2‐1, Vol. 3. World Agro Center, pp. 7–81. https://cran.r-project.org/package=vegan

Oliveira, J.M.M. , Henriques, I. , Read, D.S. , Gweon, H.S. , Morgado, R.G. , Peixoto, S. et al. (2021) Gut and faecal bacterial community of the terrestrial isopod Porcellionides pruinosus: potential use for monitoring exposure scenarios. Ecotoxicology, 30, 2096–2108. PubMed

Petrullo, L. , Ren, T. , Wu, M. , Boonstra, R. , Palme, R. , Boutin, S. et al. (2022) Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels. Scientific Reports, 12, 2605. PubMed PMC

Pfeifenschneider, J. , Brautaset, T. & Wendisch, V.F. (2017) Methanol as carbon substrate in the bio‐economy: metabolic engineering of aerobic methylotrophic bacteria for production of value‐added chemicals. Biofuels, Bioproducts and Biorefining, 11, 719–731.

Pinheiro, J.P.S. , Windsor, F.M. , Wilson, R.W. & Tyler, C.R. (2021) Global variation in freshwater physico‐chemistry and its influence on chemical toxicity in aquatic wildlife. Biological Reviews, 96, 1528–1546. PubMed

Plahuta, M. , Tišler, T. , Toman, M.J. & Pintar, A. (2017) Toxic and endocrine disrupting effects of wastewater treatment plant influents and effluents on a freshwater isopod Asellus aquaticus (Isopoda, Crustacea). Chemosphere, 174, 342–353. PubMed

Pruneau, L. , Moumène, A. , Meyer, D.F. , Marcelino, I. , Lefrançois, T. & Vachiéry, N. (2014) Understanding Anaplasmataceae pathogenesis using “omics” approaches. Frontiers in Cellular and Infection Microbiology, 4, 86. PubMed PMC

Qin, Y. , Havulinna, A.S. , Liu, Y. , Jousilahti, P. , Ritchie, S.C. , Tokolyi, A. et al. (2022) Combined effects of host genetics and diet on human gut microbiota and incident disease in a single population cohort. Nature Genetics, 54, 134–142. PubMed PMC

Reid, A.J. , Carlson, A.K. , Creed, I.F. , Eliason, E.J. , Gell, P.A. , Johnson, P.T.J. et al. (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews of the Cambridge Philosophical Society, 94, 849–873. PubMed

Ren, X. , Lee, Y.J. , Han, H.J. & Kim, I.S. (2009) Cellular effect evaluation of micropollutants using transporter functions of renal proximal tubule cells. Chemosphere, 77, 968–974. PubMed

Ribeiro, Â.M. , Puetz, L. , Pattinson, N.B. , Dalén, L. , Deng, Y. , Zhang, G. et al. (2019) 31° south: the physiology of adaptation to arid conditions in a passerine bird. Molecular Ecology, 28, 3709–3721. PubMed

Rocca, J.D. , Simonin, M. , Blaszczak, J.R. , Ernakovich, J.G. , Gibbons, S.M. , Midani, F.S. et al. (2019) The microbiome stress project: toward a global meta‐analysis of environmental stressors and their effects on microbial communities. Frontiers in Microbiology, 9, 3272. PubMed PMC

Rodríguez, J. , Gallampois, C.M.J. , Haglund, P. , Timonen, S. & Rowe, O. (2021) Bacterial communities as indicators of environmental pollution by POPs in marine sediments. Environmental Pollution, 268, 115690. PubMed

Rodríguez, J. , Gallampois, C.M.J. , Timonen, S. , Andersson, A. , Sinkko, H. , Haglund, P. et al. (2018) Effects of organic pollutants on bacterial communities under future climate change scenarios. Frontiers in Microbiology, 9, 2926. PubMed PMC

Ryan, R.P. , Monchy, S. , Cardinale, M. , Taghavi, S. , Crossman, L. , Avison, M.B. et al. (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas . Nature Reviews Microbiology, 7, 514–525. PubMed

Ryu, E.P. & Davenport, E.R. (2022) Host genetic determinants of the microbiome across animals: from Caenorhabditis elegans to cattle. Annual Review of Animal Biosciences, 10, 203–226. PubMed PMC

Salo, T. , Stamm, C. , Burdon, F.J. , Räsänen, K. & Seppälä, O. (2017) Resilience to heat waves in the aquatic snail Lymnaea stagnalis: additive and interactive effects with micropollutants. Freshwater Biology, 62, 1831–1846.

Salter, S.J. , Cox, M.J. , Turek, E.M. , Calus, S.T. , Cookson, W.O. , Moffatt, M.F. et al. (2014) Reagent and laboratory contamination can critically impact sequence‐based microbiome analyses. BMC Biology, 12, 87. PubMed PMC

Schindelin, J. , Arganda‐Carreras, I. , Frise, E. , Kaynig, V. , Longair, M. , Pietzsch, T. et al. (2012) Fiji: an open‐source platform for biological‐image analysis. Nature Methods, 9, 676–682. PubMed PMC

Schwarzenbach, R.P. , Escher, B.I. , Fenner, K. , Hofstetter, T.B. , Johnson, C.A. , von Gunten, U. et al. (2006) The challenge of micropollutants in aquatic systems. Science (New York, N.Y.), 313, 1072–1077. PubMed

Secombe, K.R. , Al‐Qadami, G.H. , Subramaniam, C.B. , Bowen, J.M. , Scott, J. , Van Sebille, Y.Z.A. et al. (2021) Guidelines for reporting on animal fecal transplantation (GRAFT) studies: recommendations from a systematic review of murine transplantation protocols. Gut Microbes, 13, 1979878. PubMed PMC

Sehnal, L. , Brammer‐Robbins, E. , Wormington, A.M. , Blaha, L. , Bisesi, J. , Larkin, I. et al. (2021) Microbiome composition and function in aquatic vertebrates: small organisms making big impacts on aquatic animal health. Frontiers in Microbiology, 12, 567408. PubMed PMC

Sender, R. , Fuchs, S. & Milo, R. (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14, e1002533. PubMed PMC

Sepulveda, J. & Moeller, A.H. (2020) The effects of temperature on animal gut microbiomes. Frontiers in Microbiology, 11, 384. PubMed PMC

Stamm, C. , Räsänen, K. , Burdon, F.J. , Altermatt, F. , Jokela, J. , Joss, A. et al. (2016) Chapter four—unravelling the impacts of micropollutants in aquatic ecosystems: interdisciplinary studies at the interface of large‐scale ecology. In: Dumbrell, A.J. , Kordas, R.L. & Woodward, G. (Eds.) Advances in ecological research, Cambridge, MA: Academic Press, pp. 183–223.

Sullam, K.E. , Essinger, S.D. , Lozupone, C.A. , O'Connor, M.P. , Rosen, G.L. , Knight, R. et al. (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta‐analysis. Molecular Ecology, 21, 3363–3378. PubMed PMC

Suzuki, T.A. (2017) Links between natural variation in the microbiome and host fitness in wild mammals. Integrative and Comparative Biology, 57, 756–769. PubMed

Taddei, A. , Räsänen, K. & Burdon, F.J. (2021) Size‐dependent sensitivity of stream amphipods indicates population‐level responses to chemical pollution. Freshwater Biology, 66, 765–784.

Tak, E.J. , Kim, P.S. , Hyun, D.W. , Kim, H.S. , Lee, J.Y. , Kang, W. et al. (2018) Phenotypic and genomic properties of Brachybacterium vulturis sp. nov. and Brachybacterium avium sp. nov. Frontiers in Microbiology, 9, 1809. PubMed PMC

Tavalire, H.F. , Christie, D.M. , Leve, L.D. , Ting, N. , Cresko, W.A. & Bohannan, B.J.M. (2021) Shared environment and genetics shape the gut microbiome after infant adoption. MBio, 12, e00548‐21. Available from: 10.1128/mbio.00548-00521 PubMed DOI PMC

Therneau, T. (2023) A package for survival analysis in R. R package version 3.5–7. https://CRANR-projectorg/package=survival

Tuomainen, U. & Candolin, U. (2011) Behavioural responses to human‐induced environmental change. Biological Reviews, 86, 640–657. PubMed

Vandenbergh, G.F. , Adriaens, D. , Verslycke, T. & Janssen, C.R. (2003) Effects of 17 alpha‐ethinylestradiol on sexual development of the amphipod Hyalella azteca . Ecotoxicology and Environmental Safety, 54, 216–222. PubMed

Vandeputte, D. , De Commer, L. , Tito, R.Y. , Kathagen, G. , Sabino, J. , Vermeire, S. et al. (2021) Temporal variability in quantitative human gut microbiome profiles and implications for clinical research. Nature Communications, 12, 6740. PubMed PMC

Verovnik, R. & Konec, M. (2019) Chapter 11—Asellus aquaticus: a model system for historical biogeography. In: White, W.B. , Culver, D.C. & Pipan, T. (Eds.) Encyclopedia of caves (third edition), Cambridge, MA: Academic Press, pp. 76–84.

Verovnik, R. , Sket, B. & Trontelj, P. (2005) The colonization of Europe by the freshwater crustacean Asellus aquaticus (Crustacea: Isopoda) proceeded from ancient refugia and was directed by habitat connectivity. Molecular Ecology, 14, 4355–4369. PubMed

Voolstra, C.R. & Ziegler, M. (2020) Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. BioEssays, 42, 2000004. PubMed

Wagener, C. , Mohanty, N.P. & Measey, J. (2020) The gut microbiome facilitates ecological adaptation in an invasive vertebrate. bioRxiv preprint. 10.1101/2020.12.10.418954 DOI

Wang, J.M. , Bai, J. , Zheng, F.Y. , Ling, Y. , Li, X. , Wang, J. et al. (2020) Diversity of the gut microbiome in three grasshopper species using 16S rRNA and determination of cellulose digestibility. PeerJ, 8, e10194. PubMed PMC

Watts, M.M. , Pascoe, D. & Carroll, K. (2002) Population responses of the freshwater amphipod Gammarus pulex (L.) to an environmental estrogen, 17α‐ethinylestradiol. Environmental Toxicology and Chemistry, 21, 445–450. PubMed

Weis, J.S. , Angela, C. & Rao, K.R. (1992) Effects of pollutants on molting and regeneration in Crustacea. American Zoologist, 32, 495–500.

Wickham, H. (2009) ggplot2: elegant graphics for data analysis (use R). New York: Springer‐Verlag.

Wilkes, R.A. & Aristilde, L. (2017) Degradation and metabolism of synthetic plastics and associated products by Pseudomonas sp.: capabilities and challenges. Journal of Applied Microbiology, 123, 582–593. PubMed

Woodward, G. , Perkins, D.M. & Brown, L.E. (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365, 2093–2106. PubMed PMC

WWF . (2022) Living planet report. https://livingplanet.panda.org/en-US/

Youngblut, N.D. , Reischer, G.H. , Walters, W. , Schuster, N. , Walzer, C. , Stalder, G. et al. (2019) Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nature Communications, 10, 2200. PubMed PMC

Yun, J.‐H. , Roh, S.W. , Whon, T.W. , Jung, M.‐J. , Kim, M.‐S. , Park, D.‐S. et al. (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology, 80, 5254–5264. PubMed PMC

Zhang, G. , Zeng, G. , Cai, X. , Deng, S. , Luo, H. & Sun, G. (2007) Brachybacterium zhongshanense sp. nov., a cellulose‐decomposing bacterium from sediment along the Qijiang River, Zhongshan City, China. International Journal of Systematic and Evolutionary Microbiology, 57, 2519–2524. PubMed

Zhu, W. , Yang, D. , Chang, L. , Zhang, M. , Zhu, L. & Jiang, J. (2022) Animal gut microbiome mediates the effects of antibiotic pollution on an artificial freshwater system. Journal of Hazardous Materials, 425, 127968. PubMed

Ziegler, M. , Grupstra, C.G.B. , Barreto, M.M. , Eaton, M. , BaOmar, J. , Zubier, K. et al. (2019) Coral bacterial community structure responds to environmental change in a host‐specific manner. Nature Communications, 10, 3092. PubMed PMC

Zimmer, M. & Bartholmé, S. (2003) Bacterial endosymbionts in Asellus aquaticus (Isopoda) and Gammarus pulex (Amphipoda) and their contribution to digestion. Limnology and Oceanography, 48, 2208–2213.

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