Cancer and One Health: tumor-bearing individuals can act as super spreaders of symbionts in communities.

Sophie Tissot, Jordan Meliani, Matthew Chee, Aurora M Nedelcu, Justine Boutry, Jácint Tökölyi, Rodrigo Hamede, Benjamin Roche, Beata Ujvari, Frédéric Thomas, Antoine M Dujon
Author Information
  1. Sophie Tissot: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France. sophie.tissot@ird.fr.
  2. Jordan Meliani: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  3. Matthew Chee: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  4. Aurora M Nedelcu: Department of Biology, University of New Brunswick, Fredericton, New Brunswick, Canada.
  5. Justine Boutry: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  6. Jácint Tökölyi: MTA-DE "Momentum" Ecology, Evolution and Developmental Biology Research Group, Department of Evolutionary Zoology, University of Debrecen, 4032, Debrecen, Hungary.
  7. Rodrigo Hamede: School of Natural Sciences, University of Tasmania, Hobart, TAS, Australia.
  8. Benjamin Roche: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  9. Beata Ujvari: School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Victoria, Australia.
  10. Frédéric Thomas: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  11. Antoine M Dujon: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.

Abstract

Recent theoretical advances in the One Health approach have suggested that cancer pathologies should be given greater consideration, as cancers often render their hosts more vulnerable to infectious agents, which could turn them into super spreaders within ecosystems. Although biologically plausible, this hypothesis has not yet been validated experimentally. Using a community of cnidarians of the Hydra genus (Hydra oligactis, Hydra viridissima, Hydra vulgaris) and a commensal ciliate species (Kerona pediculus) that colonizes them, we tested whether tumoral polyps of H. oligactis, compared to healthy ones, played an amplifying role in the number of ciliates, potentially resulting in a higher likelihood of infection for other community members through spillovers. Our results indicate that K. pediculus has a higher proliferation rate on tumoral polyps of H. oligactis than on healthy ones, which results in the infestation of other hydras. However, the magnitude of the spillover differed between recipient species. This study provides to our knowledge the first elements of proof of concept that tumoral individuals in communities could act as super spreaders of symbionts within and between species, and thus affect biotic interactions and dynamics in ecosystems.

Keywords

References

  1. Trends Ecol Evol. 2013 Nov;28(11):628-35 [PMID: 23972467]
  2. Philos Trans R Soc Lond B Biol Sci. 2017 Jan 19;372(1712): [PMID: 27920388]
  3. Nat Ecol Evol. 2018 Jul;2(7):1065-1070 [PMID: 29784981]
  4. Nat Ecol Evol. 2017 Nov;1(11):1592-1595 [PMID: 29066812]
  5. Nat Commun. 2014 Jun 24;5:4222 [PMID: 24957317]
  6. Sci Rep. 2023 May 8;13(1):7449 [PMID: 37156860]
  7. Nat Rev Microbiol. 2023 Jan;21(1):6-20 [PMID: 35999468]
  8. Proc Biol Sci. 2019 Jan 16;286(1894):20182434 [PMID: 30963883]
  9. Evol Appl. 2021 Oct 08;14(11):2571-2575 [PMID: 34815739]
  10. iScience. 2022 Aug 31;25(10):105034 [PMID: 36147948]
  11. PLoS Pathog. 2020 Mar 19;16(3):e1008375 [PMID: 32191776]
  12. Sci Total Environ. 2022 Jan 10;803:149923 [PMID: 34487898]
  13. Lancet Microbe. 2023 May;4(5):e297 [PMID: 36848921]
  14. Nat Rev Genet. 2024 Feb;25(2):142-157 [PMID: 37749210]
  15. Zoonoses Public Health. 2021 Sep;68(6):563-577 [PMID: 34018336]
  16. Transl Oncol. 2020 Jul;13(7):100759 [PMID: 32353791]
  17. Int J Environ Res Public Health. 2022 Jan 14;19(2): [PMID: 35055715]
  18. Environ Int. 2021 Apr;149:106391 [PMID: 33515955]
  19. Proc Biol Sci. 2024 Feb 14;291(2016):20232666 [PMID: 38351808]
  20. Mol Phylogenet Evol. 2010 Oct;57(1):403-10 [PMID: 20601008]
  21. Evol Appl. 2024 Aug 02;17(8):e13763 [PMID: 39100750]
  22. Int J Parasitol. 2013 Nov;43(12-13):1079-88 [PMID: 23892130]
  23. Lancet. 2021 Feb 27;397(10276):792-793 [PMID: 33640059]

Grants

  1. ANR-23-CE13-0007/ANR EVOSEXCAN

MeSH Term

Animals
Symbiosis
Neoplasms
Hydra
One Health
Ecosystem
Ciliophora

Word Cloud

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