Trade-off between photosymbiosis and innate immunity influences cnidarian's response to pathogenic bacteria

Proc Biol Sci. 2024 Oct;291(2032):20240428. doi: 10.1098/rspb.2024.0428. Epub 2024 Oct 2.

Abstract

Mutualistic relationships with photosynthetic organisms are common in cnidarians, which form an intracellular symbiosis with dinoflagellates in the family Symbiodiniaceae. The establishment and maintenance of these symbionts are associated with the suppression of key host immune factors. Because of this, there are potential trade-offs between the nutrition that cnidarian hosts gain from their symbionts and their ability to successfully defend themselves from pathogens. To investigate these potential trade-offs, we utilized the facultatively symbiotic polyps of the upside-down jellyfish Cassiopea xamachana and exposed aposymbiotic and symbiotic polyps to the pathogen Serratia marcescens. Symbiotic polyps had a lower probability of survival following S. marcescens exposure. Gene expression analyses 24 hours following pathogen exposure indicate that symbiotic animals mounted a more damaging immune response, with higher levels of inflammation and oxidative stress likely resulting in more severe disruptions to cellular homeostasis. Underlying this more damaging immune response may be differences in constitutive and pathogen-induced expression of immune transcription factors between aposymbiotic and symbiotic polyps rather than broadscale immune suppression during symbiosis. Our findings indicate that in facultatively symbiotic polyps, hosting symbionts limits C. xamachana's ability to survive pathogen exposure, indicating a trade-off between symbiosis and immunity that has potential implications for coral disease research.

Keywords: cnidarian; innate immunity; jellyfish; mutualism; symbiosis; trade-offs.

MeSH terms

  • Animals
  • Cnidaria / immunology
  • Cnidaria / physiology
  • Dinoflagellida / immunology
  • Dinoflagellida / physiology
  • Immunity, Innate*
  • Photosynthesis
  • Scyphozoa / immunology
  • Scyphozoa / microbiology
  • Scyphozoa / physiology
  • Serratia marcescens* / physiology
  • Symbiosis*