Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna

English version

Autoři: Asa Motiei ^aff001; Björn Brindefalk ^aff002; Martin Ogonowski ^aff001; Rehab El-Shehawy ^aff001; Paulina Pastuszek ^aff002; Karin Ek ^aff001; Birgitta Liewenborg ^aff001; Klas Udekwu ^aff002; Elena Gorokhova ^aff001
Působiště autorů: Department of Environmental Science & Analytical Chemistry (ACES), Stockholm University, Stockholm, Sweden ^aff001; Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden ^aff002; Aquabiota Water Research AB, Stockholm, Sweden ^aff003; Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of Freshwater Research, Drottningholm, Sweden ^aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0214833

Souhrn

It is a common view that an organism’s microbiota has a profound influence on host fitness; however, supporting evidence is lacking in many organisms. We manipulated the gut microbiome of Daphnia magna by chronic exposure to different concentrations of the antibiotic Ciprofloxacin (0.01–1 mg L^-1), and evaluated whether this affected the animals fitness and antioxidant capacity. In line with our expectations, antibiotic exposure altered the microbiome in a concentration-dependent manner. However, contrary to these expectations, the reduced diversity of gut bacteria was not associated with any fitness detriment. Moreover, the growth-related parameters correlated negatively with microbial diversity; and, in the daphnids exposed to the lowest Ciprofloxacin concentrations, the antioxidant capacity, growth, and fecundity were even higher than in control animals. These findings suggest that Ciprofloxacin exerts direct stimulatory effects on growth and reproduction in the host, while microbiome- mediated effects are of lesser importance. Thus, although microbiome profiling of Daphnia may be a sensitive tool to identify early effects of antibiotic exposure, disentangling direct and microbiome-mediated effects on the host fitness is not straightforward.

Klíčová slova:

Bacteria – Antibiotics – Microbiome – Gut bacteria – Antioxidants – Fecundity – Shannon index – Daphnia

Zdroje

1. O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006;7: 688–693. doi: 10.1038/sj.embor.7400731 16819463

2. Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host–microbiota mutualism. Nat Rev Microbiol. 2011;9: 233–243. doi: 10.1038/nrmicro2536 21358670

3. Rosenfeld CS. Gut Dysbiosis in Animals Due to Environmental Chemical Exposures. Front Cell Infect Microbiol. 2017;7. doi: 10.3389/fcimb.2017.00396 28936425

4. Lee W-J, Hase K. Gut microbiota-generated metabolites in animal health and disease. Nat Chem Biol. 2014;10: 416–424. doi: 10.1038/nchembio.1535 24838170

5. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110: 3229–3236. doi: 10.1073/pnas.1218525110 23391737

6. Kamada N, Chen GY, Inohara N, Núñez G. Control of Pathogens and Pathobionts by the Gut Microbiota. Nat Immunol. 2013;14: 685–690. doi: 10.1038/ni.2608 23778796

7. Cherrington CA, Hinton M, Pearson GR, Chopra I. Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. J Appl Bacteriol. 1991;70: 161–165. doi: 10.1111/j.1365-2672.1991.tb04442.x 1902205

8. Shin R, Park JM, An J-M, Paek K-H. Ectopic Expression of Tsi1 in Transgenic Hot Pepper Plants Enhances Host Resistance to Viral, Bacterial, and Oomycete Pathogens. Mol Plant Microbe Interact. 2002;15: 983–989. doi: 10.1094/MPMI.2002.15.10.983 12437295

9. Sison-Mangus MP, Mushegian AA, Ebert D. Water fleas require microbiota for survival, growth and reproduction. ISME J. 2015;9: 59–67. doi: 10.1038/ismej.2014.116 25026374

10. Edlund A, Ek K, Breitholtz M, Gorokhova E. Antibiotic-Induced Change of Bacterial Communities Associated with the Copepod Nitocra spinipes. PLoS ONE. 2012;7: e33107. doi: 10.1371/journal.pone.0033107 22427962

11. Gorokhova E, Rivetti C, Furuhagen S, Edlund A, Ek K, Breitholtz M. Bacteria-Mediated Effects of Antibiotics on Daphnia Nutrition. Environ Sci Technol. 2015;49: 5779–5787. doi: 10.1021/acs.est.5b00833 25850437

12. Callens M, Watanabe H, Kato Y, Miura J, Decaestecker E. Microbiota inoculum composition affects holobiont assembly and host growth in Daphnia. Microbiome. 2018;6: 56. doi: 10.1186/s40168-018-0444-1 29566771

13. Gyuraszova M, Kovalcikova A, Gardlik R. Association between oxidative status and the composition of intestinal microbiota along the gastrointestinal tract. Med Hypotheses. 2017;103: 81–85. doi: 10.1016/j.mehy.2017.04.011 28571818

14. Dietrich S, Ploessl F, Bracher F, Laforsch C. Single and combined toxicity of pharmaceuticals at environmentally relevant concentrations in Daphnia magna–A multigenerational study. Chemosphere. 2010;79: 60–66. doi: 10.1016/j.chemosphere.2009.12.069 20116828

15. Brennan SJ, Brougham CA, Roche JJ, Fogarty AM. Multi-generational effects of four selected environmental oestrogens on Daphnia magna. Chemosphere. 2006;64: 49–55. doi: 10.1016/j.chemosphere.2005.11.046 16405951

16. Wollenberger L, Halling-Sørensen B, Kusk KO. Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere. 2000;40: 723–730. doi: 10.1016/s0045-6535(99)00443-9 10705550

17. Tanaka Y, Nakanishi J. Chronic effects of p-nonylphenol on survival and reproduction of Daphnia galeata: Multigenerational life table experiment. Env Toxicol. 2002;17: 487–492. doi: 10.1002/tox.10083 12242680

18. Harris KDM, Bartlett NJ, Lloyd VK. Daphnia as an Emerging Epigenetic Model Organism. Genet Res Int. 2012;2012. doi: 10.1155/2012/147892 22567376

19. Stollewerk A. The water flea Daphnia—a “new” model system for ecology and evolution? J Biol. 2010;9: 21. doi: 10.1186/jbiol212 20478012

20. Freese HM, Schink B. Composition and Stability of the Microbial Community inside the Digestive Tract of the Aquatic Crustacean Daphnia magna. Microb Ecol. 2011;62: 882. doi: 10.1007/s00248-011-9886-8 21667195

21. Qi W, Nong G, Preston JF, Ben-Ami F, Ebert D. Comparative metagenomics of Daphnia symbionts. BMC Genomics. 2009;10: 172. doi: 10.1186/1471-2164-10-172 19383155

22. Peerakietkhajorn S, Kato Y, Kasalický V, Matsuura T, Watanabe H. Betaproteobacteria Limnohabitans strains increase fecundity in the crustacean Daphnia magna: symbiotic relationship between major bacterioplankton and zooplankton in freshwater ecosystem. Environ Microbiol. 2016;18: 2366–2374. doi: 10.1111/1462-2920.12919 26014379

23. Huang D-J, Hou J-H, Kuo T-F, Lai H-T. Toxicity of the veterinary sulfonamide antibiotic sulfamonomethoxine to five aquatic organisms. Environ Toxicol Pharmacol. 2014;38: 874–880. doi: 10.1016/j.etap.2014.09.006 25461547

24. De Liguoro M, Fioretto B, Poltronieri C, Gallina G. The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere. 2009;75: 1519–1524. doi: 10.1016/j.chemosphere.2009.02.002 19269673

25. Test No. 211: Daphnia magna Reproduction Test—en—OECD [Internet]. [cited 25 Sep 2019]. Available: https://www.oecd.org/chemicalsafety/test-no-211-daphnia-magna-reproduction-test-9789264185203-en.htm

26. LeBel M. Ciprofloxacin: Chemistry, Mechanism of Action, Resistance, Antimicrobial Spectrum, Pharmacokinetics, Clinical Trials, and Adverse Reactions. Pharmacother J Hum Pharmacol Drug Ther. 1988;8: 3–30. doi: 10.1002/j.1875-9114.1988.tb04058.x 2836821

27. Castiglioni S, Bagnati R, Fanelli R, Pomati F, Calamari D, Zuccato E. Removal of Pharmaceuticals in Sewage Treatment Plants in Italy. Environ Sci Technol. 2006;40: 357–363. doi: 10.1021/es050991m 16433372

28. Lien LTQ, Hoa NQ, Chuc NTK, Thoa NTM, Phuc HD, Diwan V, et al. Antibiotics in Wastewater of a Rural and an Urban Hospital before and after Wastewater Treatment, and the Relationship with Antibiotic Use—A One Year Study from Vietnam. Int J Environ Res Public Health. 2016;13. doi: 10.3390/ijerph13060588 27314366

29. Robinson AA, Belden JB, Lydy MJ. Toxicity of fluoroquinolone antibiotics to aquatic organisms. Environ Toxicol Chem. 2005;24: 423–430. doi: 10.1897/04-210r.1 15720004

30. Grillon A, Schramm F, Kleinberg M, Jehl F. Comparative Activity of Ciprofloxacin, Levofloxacin and Moxifloxacin against Klebsiella pneumoniae, Pseudomonas aeruginosa and Stenotrophomonas maltophilia Assessed by Minimum Inhibitory Concentrations and Time-Kill Studies. Nguyen MH, editor. PLOS ONE. 2016;11: e0156690. doi: 10.1371/journal.pone.0156690 27257956

31. Collins TJ. ImageJ for microscopy. BioTechniques. 2007;43: S25–S30. doi: 10.2144/000112517 17936939

32. Straughan DJ, Lehman N. Genetic differentiation among Oregon lake populations of the Daphnia pulex species complex. J Hered. 2000;91: 8–17. doi: 10.1093/jhered/91.1.8 10739118

33. Logares R., & Feng X. Quant-iT PicoGreen Assay. Quant-IT PicoGreen Assay. 2010;

34. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13: 581–583. doi: 10.1038/nmeth.3869 27214047

35. Team RC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017. ISBN3-900051-07-0 https://www.R-project.org; 2017.

36. McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLOS ONE. 2013;8: e61217. doi: 10.1371/journal.pone.0061217 23630581

37. Ou B, Hampsch-Woodill M, Prior RL. Development and Validation of an Improved Oxygen Radical Absorbance Capacity Assay Using Fluorescein as the Fluorescent Probe. J Agric Food Chem. 2001;49: 4619–4626. doi: 10.1021/jf010586o 11599998

38. Furuhagen S, Liewenborg B, Breitholtz M, Gorokhova E. Feeding Activity and Xenobiotics Modulate Oxidative Status in Daphnia magna: Implications for Ecotoxicological Testing. Environ Sci Technol. 2014;48: 12886–12892. doi: 10.1021/es5044722 25247638

39. Kaplan EL, Meier P. Nonparametric Estimation from Incomplete Observations. Breakthroughs in Statistics. Springer, New York, NY; 1992. pp. 319–337. doi: 10.1007/978-1-4612-4380-9_25

40. Borgan Ø. Modeling Survival Data: Extending the Cox Model. Terry M. Therneau and Patricia M. Grambsch, Springer-Verlag, New York, 2000. No. of pages: xiii + 350. Price: $69.95. ISBN 0-387-98784-3. Stat Med. 2001;20: 2053–2054. doi: 10.1002/sim.956

41. Chao A, Jost L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology. 2012;93: 2533–2547. doi: 10.1890/11-1952.1 23431585

42. Gower JC. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika. 1966;53: 325–338. doi: 10.1093/biomet/53.3–4.325

43. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package [Internet]. 2018. Available: https://CRAN.R-project.org/package = vegan

44. McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40: 4288–4297. doi: 10.1093/nar/gks042 22287627

45. Eckert EM, Pernthaler J. Bacterial epibionts of Daphnia: a potential route for the transfer of dissolved organic carbon in freshwater food webs. ISME J. 2014;8: 1808–1819. doi: 10.1038/ismej.2014.39 24694716

46. Kasalický V, Jezbera J, Šimek K, Hahn MW. Limnohabitans planktonicus sp. nov., and Limnohabitans parvus sp. nov., two novel planktonic Betaproteobacteria isolated from a freshwater reservoir. Int J Syst Evol Microbiol. 2010;60: 2710–2714. doi: 10.1099/ijs.0.018952-0 20061501

47. Bowman JP. Genus XIII. Shewanella MacDonell and Colwell 1986, 355VP (Effective publication: MacDonell and Colwell 1985, 180). 2005; Available: http://ecite.utas.edu.au/39287

48. Jezbera J, Jezberová J, Koll U, Horňák K, Šimek K, Hahn MW. Contrasting trends in distribution of four major planktonic betaproteobacterial groups along a pH gradient of epilimnia of 72 freshwater habitats. FEMS Microbiol Ecol. 2012;81: 467–479. doi: 10.1111/j.1574-6941.2012.01372.x 22452571

49. Peerakietkhajorn S, Tsukada K, Kato Y, Matsuura T, Watanabe H. Symbiotic bacteria contribute to increasing the population size of a freshwater crustacean, Daphnia magna. Environ Microbiol Rep. 2015;7: 364–372. doi: 10.1111/1758-2229.12260 25534397

50. Hincal F, Gürbay A, Favier A. Biphasic Response of Ciprofloxacin in Human Fibroblast Cell Cultures. Nonlinearity Biol Toxicol Med. 2003;1: 481–492. doi: 10.1080/15401420390271083 19330132

51. Dalla Bona M, Zounková R, Merlanti R, Blaha L, De Liguoro M. Effects of enrofloxacin, ciprofloxacin, and trimethoprim on two generations of Daphnia magna. Ecotoxicol Environ Saf. 2015;113: 152–158. doi: 10.1016/j.ecoenv.2014.11.018 25497771

52. Purswani MU, Eckert SJ, Arora HK, Noel GJ. Effect of ciprofloxacin on lethal and sublethal challenge with endotoxin and on early cytokine responses in a murine in vivo model. J Antimicrob Chemother. 2002;50: 51–58. doi: 10.1093/jac/dkf091 12096006

53. Gürbay A, Hıncal F. Ciprofloxacin‐Induced Glutathione Redox Status Alterations in Rat Tissues. Drug Chem Toxicol. 2004;27: 233–242. doi: 10.1081/dct-120037504 15478945

54. Gürbay A, Gonthier B, Daveloose D, Favier A, Hincal F. Microsomal metabolism of ciprofloxacin generates free radicals. Free Radic Biol Med. 2001;30: 1118–1121. doi: 10.1016/s0891-5849(01)00508-1 11369501

55. Oliveira MF, Geihs MA, França TFA, Moreira DC, Hermes-Lima M. Is “Preparation for Oxidative Stress” a Case of Physiological Conditioning Hormesis? Front Physiol. 2018;9. doi: 10.3389/fphys.2018.00945 30116197

56. Crumplin GC, Smith JT. Nalidixic Acid: an Antibacterial Paradox. Antimicrob Agents Chemother. 1975;8: 251–261. doi: 10.1128/aac.8.3.251 1101818

57. Ouattara AS, Assih EA, Thierry S, Cayol J-L, Labat M, Monroy O, et al. Bosea minatitlanensis sp. nov., a strictly aerobic bacterium isolated from an anaerobic digester. Int J Syst Evol Microbiol. 2003;53: 1247–1251. doi: 10.1099/ijs.0.02540-0 13130002

58. Yan L, Liu D, Wang X-H, Wang Y, Zhang B, Wang M, et al. Bacterial plasmid-mediated quinolone resistance genes in aquatic environments in China. Sci Rep. 2017;7. doi: 10.1038/srep40610 28094345

59. Peerakietkhajorn S, Tsukada K, Kato Y, Matsuura T, Watanabe H. Symbiotic bacteria contribute to increasing the population size of a freshwater crustacean, Daphnia magna. Environ Microbiol Rep. 2015;7: 364–372. doi: 10.1111/1758-2229.12260 25534397

60. Fink P, Pflitsch C, Marin K. Dietary Essential Amino Acids Affect the Reproduction of the Keystone Herbivore Daphnia pulex. PLOS ONE. 2011;6: e28498. doi: 10.1371/journal.pone.0028498 22163027

61. Taipale SJ, Brett MT, Pulkkinen K, Kainz MJ. The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction, and lipid composition. FEMS Microbiol Ecol. 2012;82: 50–62. doi: 10.1111/j.1574-6941.2012.01406.x 22564190

62. Wacker A, Elert E von. Polyunsaturated Fatty Acids: Evidence for Non-Substitutable Biochemical Resources in Daphnia Galeata. Ecology. 82: 2507–2520. doi: 10.1890/0012-9658(2001)082[2507:PFAEFN]2.0.CO;2

63. Sison-Mangus MP, Metzger CMJA, Ebert D. Host genotype-specific microbiota do not influence the susceptibility of D. magna to a bacterial pathogen. Sci Rep. 2018;8: 9407. doi: 10.1038/s41598-018-27681-x 29925845

64. Shivlata L, Satyanarayana T. Thermophilic and alkaliphilic Actinobacteria: biology and potential applications. Front Microbiol. 2015;6. doi: 10.3389/fmicb.2015.01014 26441937

65. Chater KF, Biró S, Lee KJ, Palmer T, Schrempf H. The complex extracellular biology of Streptomyces. FEMS Microbiol Rev. 2010;34: 171–198. doi: 10.1111/j.1574-6976.2009.00206.x 20088961

Článek Evaluation of rice wild relatives as a source of traits for adaptation to iron toxicity and enhanced grain quality

Článek In vivo elongation of thin filaments results in heart failure

Článek Residential neighbourhood greenspace is associated with reduced risk of cardiovascular disease: A prospective cohort study

Článek Carotid plaques and neurological impairment in patients with acute cerebral infarction

Článek Modelling of amino acid turnover in the horse during training and racing: A basis for developing a novel supplementation strategy

Článek Trends of litter decomposition and soil organic matter stocks across forested swamp environments of the southeastern US

Článek Plasma proteome profiling of freshwater and seawater life stages of rainbow trout (Oncorhynchus mykiss)

Článek Link-centric analysis of variation by demographics in mobile phone communication patterns

Článek Lateral pressure equalisation as a principle for designing support surfaces to prevent deep tissue pressure ulcers

Článek Development of a risk score for prediction of poor treatment outcomes among patients with multidrug-resistant tuberculosis

Článek Discovery of Jogalong virus, a novel hepacivirus identified in a Culex annulirostris (Skuse) mosquito from the Kimberley region of Western Australia

Článek Proof-of-concept for a non-invasive, portable, and wireless device for cardiovascular monitoring in pediatric patients