Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite.

Veronica M Sinotte, Justinn Renelies-Hamilton, Sergio Andreu-Sánchez, Mireille Vasseur-Cognet, Michael Poulsen
Author Information
  1. Veronica M Sinotte: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen East, Denmark. ORCID
  2. Justinn Renelies-Hamilton: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen East, Denmark.
  3. Sergio Andreu-Sánchez: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen East, Denmark. ORCID
  4. Mireille Vasseur-Cognet: UMR IRD 242, UPEC, CNRS 7618, UPMC 113, INRAe 1392, Paris 7 113, Institute of Ecology and Environmental Sciences of Paris, Bondy, France. ORCID
  5. Michael Poulsen: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen East, Denmark. ORCID

Abstract

Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite . We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.

Keywords

Associated Data

figshare | 10.6084/m9.figshare.22047479.v1; 10.6084/m9.figshare.22047467.v1; 10.6084/m9.figshare.22047470.v3; 10.6084/m9.figshare.22047539.v1; 10.6084/m9.figshare.c.6845629

References

  1. Nat Mach Intell. 2020 Jan;2(1):56-67 [PMID: 32607472]
  2. Science. 2018 Oct 26;362(6413):453-457 [PMID: 30361372]
  3. Proc Biol Sci. 2023 Oct 25;290(2009):20231559 [PMID: 37848067]
  4. ISME J. 2017 Dec;11(12):2639-2643 [PMID: 28731476]
  5. Environ Microbiol Rep. 2019 Apr;11(2):196-205 [PMID: 30556304]
  6. Commun Biol. 2022 Jan 13;5(1):44 [PMID: 35027667]
  7. Science. 2015 Apr 24;348(6233):392-4 [PMID: 25908807]
  8. Environ Microbiol Rep. 2016 Oct;8(5):630-640 [PMID: 27273758]
  9. Am Nat. 1997 Jul;150 Suppl 1:S80-99 [PMID: 18811314]
  10. Front Microbiol. 2017 Oct 10;8:1942 [PMID: 29067008]
  11. Mol Ecol. 2014 Sep;23(18):4631-44 [PMID: 25066007]
  12. Gut Microbes. 2021 Jan-Dec;13(1):1-17 [PMID: 33406976]
  13. Mol Ecol. 2020 Jan;29(2):308-324 [PMID: 31788887]
  14. Nature. 2017 Aug 2;548(7665):43-51 [PMID: 28770836]
  15. Front Microbiol. 2016 Feb 17;7:171 [PMID: 26925043]
  16. Nat Rev Microbiol. 2014 Mar;12(3):168-80 [PMID: 24487819]
  17. Microb Ecol. 2016 Jan;71(1):207-20 [PMID: 26518432]
  18. J Econ Entomol. 2015 Feb;108(1):266-73 [PMID: 26470129]
  19. Appl Environ Microbiol. 2018 Feb 14;84(5): [PMID: 29269491]
  20. Proc Biol Sci. 2023 Jun 28;290(2001):20230619 [PMID: 37339742]
  21. PNAS Nexus. 2023 Jul 04;2(7):pgad222 [PMID: 37457894]
  22. Microbiome. 2022 May 27;10(1):78 [PMID: 35624491]
  23. Proc Biol Sci. 2020 Sep 9;287(1934):20200820 [PMID: 32873208]
  24. Nat Ecol Evol. 2022 Jan;6(1):77-87 [PMID: 34949814]
  25. Nat Rev Microbiol. 2010 Mar;8(3):218-30 [PMID: 20157340]
  26. Nat Methods. 2016 Jul;13(7):581-3 [PMID: 27214047]
  27. Eur J Nutr. 2018 Feb;57(1):1-24 [PMID: 28393285]
  28. Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14887-92 [PMID: 12386341]
  29. Curr Biol. 2018 Feb 19;28(4):649-654.e2 [PMID: 29429621]
  30. Environ Microbiol. 2010 Aug;12(8):2120-32 [PMID: 21966907]
  31. Syst Appl Microbiol. 2015 Oct;38(7):472-82 [PMID: 26283320]
  32. Antonie Van Leeuwenhoek. 2018 Apr;111(4):573-587 [PMID: 29127624]
  33. Microbiome. 2018 Dec 17;6(1):226 [PMID: 30558668]
  34. Curr Biol. 2019 Nov 4;29(21):3728-3734.e4 [PMID: 31630948]
  35. iScience. 2019 Dec 20;22:380-391 [PMID: 31812808]
  36. PLoS Comput Biol. 2015 May 07;11(5):e1004226 [PMID: 25950956]
  37. Appl Environ Microbiol. 2014 Dec;80(23):7378-87 [PMID: 25239900]
  38. Nat Ecol Evol. 2019 Aug;3(8):1172-1183 [PMID: 31285574]
  39. Sci Adv. 2017 Mar 29;3(3):e1600513 [PMID: 28435856]
  40. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  41. Appl Environ Microbiol. 2014 Apr;80(7):2261-9 [PMID: 24487532]
  42. Nature. 2012 Sep 13;489(7415):231-41 [PMID: 22972296]
  43. Science. 2022 Jun 10;376(6598):1220-1223 [PMID: 35679413]
  44. Biol Rev Camb Philos Soc. 2018 Feb;93(1):28-54 [PMID: 28508537]
  45. Trends Microbiol. 2018 Jul;26(7):557-559 [PMID: 29752168]
  46. Mol Ecol. 2014 Mar;23(6):1268-1283 [PMID: 24304129]
  47. Nat Rev Microbiol. 2022 Feb;20(2):109-121 [PMID: 34453137]
  48. mSphere. 2019 May 15;4(3): [PMID: 31092601]
  49. ISME J. 2016 Aug;10(8):1866-76 [PMID: 26872040]
  50. PLoS Biol. 2021 Feb 19;19(2):e3001116 [PMID: 33606675]
  51. FEMS Microbiol Rev. 2013 Sep;37(5):699-735 [PMID: 23692388]
  52. Microbiome. 2021 Nov 4;9(1):216 [PMID: 34732245]
  53. Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14500-5 [PMID: 25246537]
  54. Appl Environ Microbiol. 2020 Dec 18;87(5): [PMID: 33355101]
  55. Environ Microbiol. 2016 May;18(5):1440-51 [PMID: 26346907]
  56. Bioinform Adv. 2021 Sep 19;1(1):vbab020 [PMID: 36700109]

MeSH Term

Animals
Isoptera
Biological Evolution
Microbiota
Fungi
Agriculture
Symbiosis
Phylogeny

Word Cloud

Created with Highcharts 10.0.0transmissionoffspringmicrobesverticalcomplexgutbacterialcoloniestermitecolonycoevolutionsymbiontshostcommunitiesstrainsfungus-farmingmicrobiomereproductivesmicrobiomesMutualisticcanmediatedgenerationsTermitesevolutionaryhistoriesindicativemixed-modedocumentcongruentacrossparentfourpedigreesshow44%including80generapedigree-specificconsistentlyinheritedgodemonstrateachievedcolony-foundingselectivelyenrichedsetnon-randomenvironmentallysensitivetermite-specificorigintransferworkershighfidelitypriorityeffectsappearinfluencecompositionestablishingTermitethussecurespecificco-evolvedcriticalExtensiveyetimperfectinheritanceimpliesmaturingbenefitsacquiringenvironmentalcomplementcombinationsfungusverticallytransmittedmodeemergingprevailingstrategyhostsassembleadaptiveSelectiveenrichmentfoundingreproductiveallowsextensiveMacrotermitinaemicrobiotasocialinsectssuperorganismsymbiosis

Similar Articles

Cited By