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Environmental microbiology reports
Jun, 2024;16 (3): e13252.

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

Terézia Horváthová, Elvira Lafuente, Jo-Anne Bartels, Jesper Wallisch, Christoph Vorburger
Author Information
  1. Terézia Horváthová: Department of Aquatic Ecology, Eawag, Dübendorf, Switzerland. ORCID
  2. Elvira Lafuente: Department of Aquatic Ecology, Eawag, Dübendorf, Switzerland.
  3. Jo-Anne Bartels: Department of Aquatic Ecology, Eawag, Dübendorf, Switzerland.
  4. Jesper Wallisch: Department of Aquatic Ecology, Eawag, Dübendorf, Switzerland.
  5. Christoph Vorburger: Department of Aquatic Ecology, Eawag, Dübendorf, Switzerland.
PMID: 38783543 DOI: 10.1111/1758-2229.13252

Abstract

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.

References

  1. Nat Commun. 2021 Aug 26;12(1):5141 [PMID: 34446709]
  2. Mol Ecol. 2012 Jul;21(13):3363-78 [PMID: 22486918]
  3. Front Microbiol. 2018 Nov 30;9:2926 [PMID: 30555447]
  4. J Anim Ecol. 2012 May;81(3):583-93 [PMID: 22269070]
  5. Zoology (Jena). 2018 Apr;127:1-19 [PMID: 29599012]
  6. J Appl Microbiol. 2017 Sep;123(3):582-593 [PMID: 28419654]
  7. Gut Microbes. 2021 Jan-Dec;13(1):1979878 [PMID: 34586011]
  8. Environ Toxicol Chem. 2006 Feb;25(2):452-7 [PMID: 16519306]
  9. Sci Rep. 2022 Feb 16;12(1):2605 [PMID: 35173201]
  10. FEMS Microbiol Ecol. 2020 Aug 1;96(8): [PMID: 32573725]
  11. FEMS Microbiol Ecol. 2019 May 1;95(5): [PMID: 30997495]
  12. Annu Rev Anim Biosci. 2022 Feb 15;10:203-226 [PMID: 35167316]
  13. Nat Commun. 2019 May 16;10(1):2200 [PMID: 31097702]
  14. Ecotoxicol Environ Saf. 2003 Feb;54(2):216-22 [PMID: 12550100]
  15. Front Microbiol. 2021 Mar 11;12:567408 [PMID: 33776947]
  16. FEMS Microbiol Ecol. 2016 May;92(5):fiw063 [PMID: 27004796]
  17. Oecologia. 1993 Dec;96(3):304-309 [PMID: 28313643]
  18. Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190589 [PMID: 32772662]
  19. Nat Ecol Evol. 2022 Jan;6(1):77-87 [PMID: 34949814]
  20. mBio. 2021 Mar 30;12(2): [PMID: 33785620]
  21. Ecol Lett. 2014 Aug;17(8):932-41 [PMID: 24811760]
  22. PLoS One. 2013 Apr 22;8(4):e61217 [PMID: 23630581]
  23. Nat Commun. 2021 Nov 18;12(1):6740 [PMID: 34795283]
  24. PeerJ. 2020 Nov 05;8:e10194 [PMID: 33194406]
  25. Front Microbiol. 2022 Jul 05;13:703183 [PMID: 35865927]
  26. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  27. J Therm Biol. 2019 May;82:222-228 [PMID: 31128651]
  28. Sci Total Environ. 2003 Dec 30;317(1-3):207-33 [PMID: 14630423]
  29. Nat Commun. 2019 Jul 12;10(1):3092 [PMID: 31300639]
  30. Front Microbiol. 2018 Aug 07;9:1809 [PMID: 30131788]
  31. Environ Toxicol Chem. 2002 Feb;21(2):445-50 [PMID: 11833814]
  32. Biol Rev Camb Philos Soc. 2019 Jun;94(3):849-873 [PMID: 30467930]
  33. Evol Appl. 2023 Mar 30;16(4):824-848 [PMID: 37124094]
  34. Q Rev Biol. 2012 Dec;87(4):325-41 [PMID: 23397797]
  35. Philos Trans R Soc Lond B Biol Sci. 2010 Jul 12;365(1549):2093-106 [PMID: 20513717]
  36. ILAR J. 2004;45(4):484-93 [PMID: 15454687]
  37. mSystems. 2021 Oct 26;6(5):e0070721 [PMID: 34581596]
  38. Zookeys. 2016 Apr 05;(577):25-41 [PMID: 27110187]
  39. Science. 2006 Aug 25;313(5790):1072-7 [PMID: 16931750]
  40. Nat Methods. 2012 Jun 28;9(7):676-82 [PMID: 22743772]
  41. Int J Syst Evol Microbiol. 2007 Nov;57(Pt 11):2519-2524 [PMID: 17978212]
  42. Nat Rev Microbiol. 2021 Oct;19(10):623-638 [PMID: 33875863]
  43. Nat Commun. 2022 Jul 1;13(1):3804 [PMID: 35778405]
  44. Environ Pollut. 2014 Sep;192:196-203 [PMID: 24967699]
  45. Glob Chang Biol. 2023 Jan;29(1):41-56 [PMID: 36251487]
  46. Nat Rev Microbiol. 2009 Jul;7(7):514-25 [PMID: 19528958]
  47. Ecol Lett. 2023 Sep;26 Suppl 1:S81-S90 [PMID: 36965002]
  48. Integr Comp Biol. 2017 Oct 1;57(4):756-769 [PMID: 28992216]
  49. Ecotoxicology. 2015 Nov;24(9):1976-95 [PMID: 26385344]
  50. Microbiome. 2018 Nov 26;6(1):209 [PMID: 30477569]
  51. Microbiome. 2022 Apr 11;10(1):58 [PMID: 35410630]
  52. Front Microbiol. 2020 Mar 10;11:384 [PMID: 32210948]
  53. Trends Ecol Evol. 2024 Feb;39(2):165-174 [PMID: 37863775]
  54. J Anim Ecol. 2019 Nov;88(11):1684-1695 [PMID: 31325164]
  55. Water Res. 2017 Mar 1;110:366-377 [PMID: 27919541]
  56. Biol Rev Camb Philos Soc. 2011 Aug;86(3):640-57 [PMID: 20977599]
  57. J Hazard Mater. 2022 Mar 5;425:127968 [PMID: 34894514]
  58. Int J Environ Res Public Health. 2019 Mar 11;16(5): [PMID: 30862023]
  59. Water Environ Res. 2019 Oct;91(10):1272-1287 [PMID: 31486195]
  60. PeerJ. 2015 Aug 18;3:e1190 [PMID: 26311208]
  61. mSphere. 2021 Jun 16;:e0050621 [PMID: 34133198]
  62. Mol Ecol. 2005 Dec;14(14):4355-69 [PMID: 16313598]
  63. Proc Biol Sci. 1998 Jun 22;265(1401):1081-90 [PMID: 9684374]
  64. Front Endocrinol (Lausanne). 2021 Mar 02;12:587608 [PMID: 33737907]
  65. mBio. 2021 Dec 21;12(6):e0249621 [PMID: 34724817]
  66. Nat Prod Rep. 2018 May 25;35(5):434-454 [PMID: 29644346]
  67. Front Cell Infect Microbiol. 2014 Jul 02;4:86 [PMID: 25072029]
  68. ISME J. 2021 Jun;15(6):1722-1734 [PMID: 33452480]
  69. Arch Environ Contam Toxicol. 2012 Jul;63(1):77-85 [PMID: 22223070]
  70. NPJ Biofilms Microbiomes. 2016 May 04;2:16003 [PMID: 28721242]
  71. J Evol Biol. 2007 May;20(3):831-44 [PMID: 17465894]
  72. Chemosphere. 2017 May;174:342-353 [PMID: 28183060]
  73. ISME J. 2020 Feb;14(2):531-543 [PMID: 31676854]
  74. Proc Natl Acad Sci U S A. 2014 Jul 1;111(26):9549-54 [PMID: 24979762]
  75. Biotechnol Biofuels. 2020 Mar 13;13:49 [PMID: 32190114]
  76. Appl Environ Microbiol. 2014 Sep;80(17):5254-64 [PMID: 24928884]
  77. Nat Rev Microbiol. 2022 Feb;20(2):109-121 [PMID: 34453137]
  78. Environ Microbiol Rep. 2024 Jun;16(3):e13252 [PMID: 38783543]
  79. Science. 2021 Jul 9;373(6551):181-186 [PMID: 34244407]
  80. Mol Ecol. 2019 Aug;28(16):3709-3721 [PMID: 31291502]
  81. PLoS Biol. 2016 Aug 19;14(8):e1002533 [PMID: 27541692]
  82. Front Microbiol. 2019 Jan 10;9:3272 [PMID: 30687263]
  83. Trends Microbiol. 2019 Feb;27(2):105-117 [PMID: 30497919]
  84. Bioessays. 2020 Jul;42(7):e2000004 [PMID: 32548850]
  85. Philos Trans R Soc Lond B Biol Sci. 2012 Jun 19;367(1596):1665-79 [PMID: 22566674]
  86. Microbiome. 2021 Jul 31;9(1):166 [PMID: 34332628]
  87. Nat Commun. 2017 Nov 20;8(1):1608 [PMID: 29151571]
  88. Neurogastroenterol Motil. 2022 Oct;34(10):e14346 [PMID: 35246905]
  89. Water Res. 2023 Feb 1;229:119413 [PMID: 36470046]
  90. FEMS Microbiol Rev. 2013 Sep;37(5):699-735 [PMID: 23692388]
  91. Environ Health Perspect. 1998 Apr;106 Suppl 2:593-611 [PMID: 9599707]
  92. Oecologia. 1980 Jan;45(3):419-420 [PMID: 28309574]
  93. Genes (Basel). 2021 Jan 07;12(1): [PMID: 33430247]
  94. Ecotoxicology. 2021 Dec;30(10):2096-2108 [PMID: 34553289]
  95. Environ Microbiol Rep. 2023 Jun;15(3):188-196 [PMID: 36779263]
  96. Environ Pollut. 2021 Jan 1;268(Pt A):115690 [PMID: 33045590]
  97. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3229-36 [PMID: 23391737]
  98. Biol Rev Camb Philos Soc. 2021 Aug;96(4):1528-1546 [PMID: 33942490]
  99. Nucleic Acids Res. 2017 Jul 3;45(W1):W180-W188 [PMID: 28449106]
  100. Chemosphere. 2019 Nov;235:498-509 [PMID: 31276864]
  101. Nat Genet. 2022 Feb;54(2):134-142 [PMID: 35115689]
  102. Chemosphere. 2009 Nov;77(7):968-74 [PMID: 19729184]
  103. Proc Natl Acad Sci U S A. 2012 May 29;109(22):8618-22 [PMID: 22529384]
  104. BMC Genomics. 2019 Jun 7;20(1):462 [PMID: 31174468]
  105. BMC Microbiol. 2020 Apr 21;20(1):100 [PMID: 32316935]
  106. BMC Biol. 2014 Nov 12;12:87 [PMID: 25387460]
  107. Ann Glob Health. 2020 Dec 03;86(1):151 [PMID: 33354517]

Grants

  1. /DUE-Mobil Grant from the University of Duisburg-Essen
  2. CZ.02.2.69/0.0/0.0/20_079/0017809/Ministry of Education, Youth and Sports of the Czech Republic
  3. 5221.00979.008.08/Eawag Academic Transition Grant
  4. /Individual Travel Grant from the Radboud University Nijmegen

MeSH Term

Animals
Fresh Water
Microbiota
Isopoda
Feces
Water Pollutants, Chemical
Bacteria
Environmental Pollution

Chemicals

Water Pollutants, Chemical
Journal Article
Article has an altmetric score of 1

Word Cloud

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