Oxygen supersaturation adds resistance to a cnidarian: Symbiodiniaceae holobiont under moderate warming in experimental settings

Arossa, Silvia; Klein, Shannon G.; Garuglieri, Elisa; Steckbauer, Alexandra; Parry, Anieka J.; Alva Garcia, Jacqueline V.; Alamoudi, Taiba; Yang, Xinyuan; Hung, Shiou-Han; Salazar, Octavio R.; Marasco, Ramona; Fusi, Marco; Aranda, Manuel; Daffonchio, Daniele; Duarte, Carlos M.

doi:10.3389/fmars.2024.1305674

Oxygen supersaturation adds resistance to a cnidarian: Symbiodiniaceae holobiont under moderate warming in experimental settings

Arossa, Silvia; Klein, Shannon G.; Garuglieri, Elisa; Steckbauer, Alexandra; Parry, Anieka J.; Alva Garcia, Jacqueline V.; Alamoudi, Taiba; Yang, Xinyuan; Hung, Shiou-Han; Salazar, Octavio R.; Marasco, Ramona; Fusi, Marco; Aranda, Manuel; Daffonchio, Daniele; Duarte, Carlos M.

Authors

Silvia Arossa

Shannon G. Klein

Elisa Garuglieri

Alexandra Steckbauer

Anieka J. Parry

Jacqueline V. Alva Garcia

Taiba Alamoudi

Xinyuan Yang

Shiou-Han Hung

Octavio R. Salazar

Ramona Marasco

Marco Fusi

Manuel Aranda

Daniele Daffonchio

Carlos M. Duarte

Abstract

Ocean warming reduces O2 solubility and increases organismal O2 demand, endangering marine life. Coastal ecosystems, however, experience O2 supersaturation during peak daytime temperatures due to metabolic cycles. Recent discoveries show that this environmental supersaturation can reduce the vulnerability of tropical species to warming by satisfying their oxygen requirements. To test whether this also occurs within the cnidarian holobiont, we elevated internal O2 in Cassiopea andromeda at nighttime (i.e. holobiont respiration prevails on Symbiodniaceae O2 production) relying on bell pulsation for ventilation, then experimentally subjected them to thermal stress (+1°C day-1). Though ecologically unrealistic, this approach verified our hypothesis and eliminated confounding factors. Holobionts were exposed to either constant levels of 100% air saturation (100AS) or nighttime supersaturation (NSS; where 100% air saturation transitioned to O2 supersaturation at nighttime). At sublethal temperatures, supersaturation mitigated reductions in holobiont size of ~ 10.37% (-33.418% ± 0.345 under 100AS vs -23.039% ± 0.687 under NSS). Supersaturation alleviated chlorophyll-a loss by 42.73% until 34°C, when counteraction of this process could not be sustained due to excessive thermal stress. Supersaturation also enriched potentially beneficial bacterial taxa of the microbiome and selected a more consistent bacterial community. Although modest, the detected effects show that a O2 surplus increased the resistance of the holobionts to thermal stress.

Citation

Arossa, S., Klein, S. G., Garuglieri, E., Steckbauer, A., Parry, A. J., Alva Garcia, J. V., Alamoudi, T., Yang, X., Hung, S.-H., Salazar, O. R., Marasco, R., Fusi, M., Aranda, M., Daffonchio, D., & Duarte, C. M. (2024). Oxygen supersaturation adds resistance to a cnidarian: Symbiodiniaceae holobiont under moderate warming in experimental settings. Frontiers in Marine Science, 11, Article 1305674. https://doi.org/10.3389/fmars.2024.1305674

Journal Article Type	Article
Acceptance Date	May 27, 2024
Online Publication Date	Jun 12, 2024
Publication Date	2024
Deposit Date	Aug 9, 2024
Publicly Available Date	Aug 9, 2024
Journal	Frontiers in Marine Science
Print ISSN	2296-7745
Publisher	Frontiers Media
Peer Reviewed	Peer Reviewed
Volume	11
Article Number	1305674
DOI	https://doi.org/10.3389/fmars.2024.1305674
Keywords	ocean warming, oxygen supersaturation, cnidarian microbiome, endosymbiosis, cnidarian