Environmental bacteria increase population growth of hydra at low temperature.

Máté Miklós, Karolina Cseri, Levente Laczkó, Gábor Kardos, Sebastian Fraune, Jácint Tökölyi
Author Information
  1. Máté Miklós: MTA-DE "Momentum" Ecology, Evolution and Developmental Biology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, Hungary.
  2. Karolina Cseri: Institute of Metagenomics, University of Debrecen, Debrecen, Hungary.
  3. Levente Laczkó: Institute of Metagenomics, University of Debrecen, Debrecen, Hungary.
  4. Gábor Kardos: Institute of Metagenomics, University of Debrecen, Debrecen, Hungary.
  5. Sebastian Fraune: Institute of Zoology and Organismic Interactions, Heinrich-Heine University, Düsseldorf, Germany.
  6. Jácint Tökölyi: MTA-DE "Momentum" Ecology, Evolution and Developmental Biology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, Hungary.

Abstract

Multicellular organisms engage in complex ecological interactions with microorganisms, some of which are harmful to the host's health and fitness (e.g., pathogens or toxin-producing environmental microbiota), while others are either beneficial or have a neutral impact (as seen in components of host-associated microbiota). Although environmental microorganisms are generally considered to have no significant impact on animal fitness, there is evidence suggesting that exposure to these microbes might be required for proper immune maturation and research in vertebrates has shown that developing in a sterile environment detrimentally impacts health later in life. However, it remains uncertain whether such beneficial effects of environmental microorganisms are present in invertebrates that lack an adaptive immune system. In the present study, we conducted an experiment with field-collected , a cold-adapted freshwater cnidarian. We cultured these organisms in normal and autoclaved lake water at two distinct temperatures: 8°C and 12°C. Our findings indicated that polyps maintained in sterilized lake water displayed reduced population growth that depended on temperature, such that the effect was only present on 8°C. To better understand the dynamics of microbial communities both inhabiting polyps and their surrounding environment we conducted 16S sequencing before and after treatment, analyzing samples from both the polyps and the water. As a result of culturing in autoclaved lake water, the polyps showed a slightly altered microbiota composition, with some microbial lineages showing significant reduction in abundance, while only a few displayed increased abundances. The autoclaved lake water was recolonized, likely from the surface of hydra polyps, by a complex albeit different community of bacteria, some of which (such as , Flavobacteriaceae) might be pathogenic to hydra. The abundance of the intracellular symbiont was positively related to hydra population size. These findings indicate that at low temperature environmental microbiota can enhance population growth rate in hydra, suggesting that environmental microorganisms can provide benefits to animals even in the absence of an adaptive immune system.

Keywords

References

  1. Mol Ecol. 2021 Mar;30(5):1206-1222 [PMID: 33465828]
  2. Science. 2002 Apr 19;296(5567):490-4 [PMID: 11964470]
  3. Sci Rep. 2017 Nov 21;7(1):15937 [PMID: 29162937]
  4. ISME J. 2014 Apr;8(4):830-40 [PMID: 24335825]
  5. J Exp Biol. 2023 Jan 1;226(1): [PMID: 36546449]
  6. Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13146-51 [PMID: 17664430]
  7. mBio. 2019 May 14;10(3): [PMID: 31088923]
  8. PLoS One. 2010 Mar 10;5(3):e9490 [PMID: 20224823]
  9. Front Immunol. 2018 Aug 22;9:1915 [PMID: 30186286]
  10. PLoS Pathog. 2020 Mar 19;16(3):e1008375 [PMID: 32191776]
  11. ISME J. 2015 Nov;9(11):2515-26 [PMID: 25909977]
  12. Science. 2011 Nov 4;334(6056):670-4 [PMID: 22053049]
  13. Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21459-21468 [PMID: 32817436]
  14. Vet Res. 2011 Feb 02;42:20 [PMID: 21314902]
  15. Front Public Health. 2018 Aug 30;6:235 [PMID: 30214898]
  16. FEMS Microbiol Ecol. 2020 Aug 1;96(8): [PMID: 32573725]
  17. Nat Commun. 2022 Jan 17;13(1):342 [PMID: 35039521]
  18. Nucleic Acids Res. 2020 Jan 8;48(D1):D445-D453 [PMID: 31586394]
  19. Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
  20. Nat Methods. 2016 Jul;13(7):581-3 [PMID: 27214047]
  21. Nat Rev Immunol. 2023 Nov;23(11):735-748 [PMID: 37138015]
  22. PLoS One. 2013 Apr 22;8(4):e61217 [PMID: 23630581]
  23. Dev Comp Immunol. 2022 Jan;126:104245 [PMID: 34453995]
  24. Nat Commun. 2020 Jul 14;11(1):3514 [PMID: 32665548]
  25. Front Microbiol. 2018 Mar 21;9:487 [PMID: 29619014]
  26. Proc Natl Acad Sci U S A. 2010 Oct 19;107(42):18067-72 [PMID: 20921390]
  27. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7927-31 [PMID: 3186697]
  28. Bioinformatics. 2018 Sep 1;34(17):i884-i890 [PMID: 30423086]
  29. Nat Biotechnol. 2020 Jun;38(6):685-688 [PMID: 32483366]
  30. ISME J. 2015 Jul;9(7):1543-56 [PMID: 25514534]
  31. Glob Chang Biol. 2023 Jan;29(1):41-56 [PMID: 36251487]
  32. Environ Microbiol. 2020 Feb;22(2):564-567 [PMID: 31849163]
  33. Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190596 [PMID: 32772667]
  34. Nat Ecol Evol. 2022 Apr;6(4):405-417 [PMID: 35256809]
  35. ISME J. 2015 Jan;9(1):59-67 [PMID: 25026374]
  36. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  37. PLoS Pathog. 2022 Oct 13;18(10):e1010841 [PMID: 36227856]
  38. Water Res. 2007 Apr;41(8):1754-62 [PMID: 17307215]
  39. Microbiome. 2022 Jun 4;10(1):85 [PMID: 35659369]
  40. Curr Opin Gastroenterol. 2015 Jan;31(1):69-75 [PMID: 25394236]
  41. Genome Biol. 2022 Apr 14;23(1):95 [PMID: 35421994]
  42. Mol Ecol. 2023 Sep;32(18):5186-5200 [PMID: 37577956]
  43. Microbiome. 2018 May 17;6(1):90 [PMID: 29773078]
  44. Nat Commun. 2017 Jul 20;8(1):86 [PMID: 28729558]
  45. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3229-36 [PMID: 23391737]
  46. mBio. 2020 Nov 17;11(6): [PMID: 33203753]
  47. Sci Total Environ. 2022 Jan 10;803:149923 [PMID: 34487898]
  48. Proc Natl Acad Sci U S A. 2018 Dec 18;115(51):E11951-E11960 [PMID: 30510004]
  49. J Exp Biol. 2023 Jun 15;226(12): [PMID: 37232216]
  50. Nat Biotechnol. 2019 Aug;37(8):852-857 [PMID: 31341288]
  51. Brief Bioinform. 2023 Jan 19;24(1): [PMID: 36617187]
  52. Mol Ecol. 2018 Apr;27(8):1992-2006 [PMID: 29411448]

Word Cloud

Created with Highcharts 10.0.0waterenvironmentalmicrobiotalakepolypshydramicroorganismsautoclavedpopulationfitnessimmunepresentgrowthtemperatureorganismscomplexecologicalinteractionshealthbeneficialimpacthost-associatedsignificantsuggestingmightenvironmentadaptivesystemconductedfreshwater8°Cfindingsdisplayedmicrobial16SsequencingabundancebacterialowcanMulticellularengageharmfulhost'segpathogenstoxin-producingotherseitherneutralseencomponentsAlthoughgenerallyconsideredanimalevidenceexposuremicrobesrequiredpropermaturationresearchvertebratesshowndevelopingsteriledetrimentallyimpactslaterlifeHoweverremainsuncertainwhethereffectsinvertebrateslackstudyexperimentfield-collectedcold-adaptedcnidarianculturednormaltwodistincttemperatures:12°CindicatedmaintainedsterilizedreduceddependedeffectbetterunderstanddynamicscommunitiesinhabitingsurroundingtreatmentanalyzingsamplesresultculturingshowedslightlyalteredcompositionlineagesshowingreductionincreasedabundancesrecolonizedlikelysurfacealbeitdifferentcommunityFlavobacteriaceaepathogenicintracellularsymbiontpositivelyrelatedsizeindicateenhancerateprovidebenefitsanimalsevenabsenceEnvironmentalincreaseCnidariaDarwinianecology

Similar Articles

Cited By