The Internal Microenvironment of the Symbiotic Jellyfish Cassiopea sp. From the Red Sea

Silvia Arossa,Anieka J Parry,Matteo Callegari,Shiou-Han Hung,Shannon G Klein,Alexandra Steckbauer,Manuel Aranda,Daniele Daffonchio,Carlos M Duarte,Alan Barozzi

doi:10.3389/fmars.2021.705915

Silvia Arossa, Anieka J Parry + Show 8 more

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https://doi.org/10.3389/fmars.2021.705915

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Abstract

The characterization of the internal microenvironment of symbiotic marine invertebrates is essential for a better understanding of the symbiosis dynamics. Microalgal symbionts (of the family: Symbiodiniaceae) influence diel fluctuations of in host O2 and pH conditions through their metabolic activities (i.e., photosynthesis and respiration). These variations may play an important role in driving oxygen budgets and energy demands of the holobiont and its responses to climate change. In situ measurements using microsensors were used to resolve the O2 and pH diel fluctuations in the oral arms of non-calcifying cnidarian model species Cassiopea sp. (the “upside-down jellyfish”), which has an obligatory association with Symbiodiniaceae. Before sunrise, the internal O2 and pH levels were substantially lower than those in ambient seawater conditions (minimum average levels: 61.92 ± 5.06 1SE μmol O2 L–1 and 7.93 ± 0.02 1SE pH units, respectively), indicating that conditions within Cassiopea’s oral arms were acidified and hypoxic relative to the surrounding seawater. Measurements performed during the afternoon revealed hyperoxia (maximum average levels: 546.22 ± 16.45 1SE μmol O2 L–1) and internal pH similar to ambient levels (8.61 ± 0.02 1SE pH units). The calculated gross photosynthetic rates of Cassiopea sp. were 0.04 ± 0.013 1SE nmol cm–2 s–1 in individuals collected at night and 0.08 ± 0.02 1SE nmol cm–2 s–1 in individuals collected during the afternoon.

Highlights

The mutualistic endosymbiosis between marine invertebrates and photosynthetic dinoflagellates represents one of the most important associations in tropical marine environments, allowing the growth of diverse, healthy and productive marine ecosystems, including coral reefs (Done et al, 1996; Knowlton et al, 2010; Davy et al, 2012; de Groot et al, 2012; Fransolet et al, 2012; Kennedy et al, 2013)
Up to 95% of the photosynthates are translocated to the host (Muscatine, 1990), including oxygen, which helps the host to produce more ATP (Jokiel, 2011) and it is used to support both symbiont and host respiration (Kühl et al, 1995)
The specimen was placed in a container filled with seawater and covered with dark black plastic to protect against artificial light, before being transferred to the Red Sea Research Center (RSRC) laboratories

Summary

Introduction

The mutualistic endosymbiosis between marine invertebrates and photosynthetic dinoflagellates represents one of the most important associations in tropical marine environments, allowing the growth of diverse, healthy and productive marine ecosystems, including coral reefs (Done et al, 1996; Knowlton et al, 2010; Davy et al, 2012; de Groot et al, 2012; Fransolet et al, 2012; Kennedy et al, 2013). The host receives organic nutrients and oxygen by the symbiont (Muscatine, 1967; Muscatine and Porter, 1977; Falkowski et al, 1984; Muscatine et al, 1984; Smith and Muscatine, 1999; Hoegh-Guldberg et al, 2007; Mortillaro et al, 2009) In these relationships a nutrient exchange between host and symbionts occurs: inorganic nutrients, such as carbon, nitrogen and phosphorous, are released by the host, taken up by the symbionts and used for their metabolic activities (e.g., carbon fixation, nitrogen assimilation and growth; Miller and Yellowlees, 1989). The photosynthesis by symbionts provides a massive contributor to the holobiont’s (i.e., host and symbionts considered together) energy demands (Gattuso et al, 1999) and oxygen budget (Jokiel, 2011)

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