The Evolution, Assembly, and Dynamics of Marine Holobionts.

The holobiont concept (i.e., multiple living beings in close symbiosis with one another and functioning as a unit) is revolutionizing our understanding of biology, especially in marine systems. The earliest marine holobiont was likely a syntrophic partnership of at least two prokaryotic members. Since then, symbiosis has enabled marine organisms to conquer all ocean habitats through the formation of holobionts with a wide spectrum of complexities. However, most scientific inquiries have focused on isolated organisms and their adaptations to specific environments. In this review, we attempt to illustrate why a holobiont perspective-specifically, the study of how numerous organisms form a discrete ecological unit through symbiosis-will be a more impactful strategy to advance our understanding of the ecology and evolution of marine life. We argue that this approach is instrumental in addressing the threats to marine biodiversity posed by the current global environmental crisis.

The Zooxanthellate Jellyfish Holobiont Cassiopea andromeda, a Source of Soluble Bioactive Compounds.

Cassiopea andromeda (Forsskål, 1775), commonly found across the Indo-Pacific Ocean, the Red Sea, and now also in the warmest areas of the Mediterranean Sea, is a scyphozoan jellyfish that hosts autotrophic dinoflagellate symbionts (family Symbiodiniaceae). Besides supplying photosynthates to their host, these microalgae are known to produce bioactive compounds as long-chain unsaturated fatty acids, polyphenols, and pigments, including carotenoids, with antioxidant properties and other beneficial biological activities. By the present study, a fractionation method was applied on the hydroalcoholic extract from two main body parts (oral arms and umbrella) of the jellyfish holobiont to obtain an improved biochemical characterization of the obtained fractions from the two body parts. The composition of each fraction (i.e., proteins, phenols, fatty acids, and pigments) as well as the associated antioxidant activity were analyzed. The oral arms proved richer in zooxanthellae and pigments than the umbrella. The applied fractionation method was effective in separating pigments and fatty acids into a lipophilic fraction from proteins and pigment-protein complexes. Therefore, the C. andromeda-dinoflagellate holobiont might be considered as a promising natural source of multiple bioactive compounds produced through mixotrophic metabolism, which are of interest for a wide range of biotechnological applications.

Reproductive cycle and gonadal output of the Lessepsian jellyfish Cassiopea andromeda in NW Sicily (Central Mediterranean Sea).

Knowledge of the reproductive strategy is a key prerequisite to predict population dynamics and potential invasiveness of both native and non-indigenous outbreak-forming species. In 2014 the Lessepsian upside-down jellyfish Cassiopea andromeda reached the harbor of Palermo (NW Sicily, Thyrrenian Sea), to date its established westernmost outpost in the Mediterranean Sea. To predict C. andromeda reproductive success in its novel habitat, gonad histology was carried out to record the number and size of mature and immature oocytes. Both male and female simultaneously presented gametes at all stages of development suggesting an asynchronous, yet apparently continuous, reproduction strategy. Indeed, oogenesis was observed throughout the year from pre-vitellogenic, vitellogenetic, and late-vitellogenetic to mature oocytes suggesting multiple reproductive events, as known in other Mediterranean Rhizostomeae. Oocytes were found from May to December, with two seasonal peaks of abundance (late spring = 392 and autumn = 272), suggesting imminent spawning events. Further, jellyfish size varied significantly throughout the year, with maximum diameter (up to 24 cm) in summer, and minimum diameter (6 cm) in winter. Small-sized jellyfish in winter belong to the new cohort, most probably arising from intense summer strobilation of polyps. Late spring fertilization, planula development, and metamorphosis, followed by polyp strobilation in the summer months, may explain the late appearance of a new jellyfish cohort, likely coincident with that recorded throughout winter.

High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters.

Ecological profiling of non-native species is essential to predict their dispersal and invasiveness potential across different areas of the world. Cassiopea is a monophyletic taxonomic group of scyphozoan mixotrophic jellyfish including C. andromeda, a recent colonizer of sheltered, shallow-water habitats of the Mediterranean Sea, such as harbors and other light-limited, eutrophic coastal habitats. To assess the ecophysiological plasticity of Cassiopea jellyfish and their potential to spread across the Mare Nostrum by secondary introductions, we investigated rapid photosynthetic responses of jellyfish to irradiance transitions-from reduced to increased irradiance conditions (as paradigm of transition from harbors to coastal, meso/oligotrophic habitats). Laboratory incubation experiments were carried out to compare oxygen fluxes and photobiological variables in Cassiopea sp. immature specimens pre-acclimated to low irradiance (PAR = 200 µmol photons m-2 s-1) and specimens rapidly exposed to higher irradiance levels (PAR = 500 µmol photons m-2 s-1). Comparable photosynthetic potential and high photosynthetic rates were measured at both irradiance values, as also shown by the rapid light curves. No significant differences were observed in terms of symbiont abundance between control and treated specimens. However, jellyfish kept at the low irradiance showed a higher content in chlorophyll a and c (0.76±0.51SD vs 0.46±0.13SD mg g-1 AFDW) and a higher Ci (amount of chlorophyll per cell) compared to jellyfish exposed to higher irradiance levels. The ratio between gross photosynthesis and respiration (P:R) was >1, indicating a significant input from the autotrophic metabolism. Cassiopea sp. specimens showed high photosynthetic performances, at both low and high irradiance, demonstrating high potential to adapt to sudden changes in light exposure. Such photosynthetic plasticity, combined with Cassiopea eurythermal tolerance and mixotrophic behavior, jointly suggest the upside-down jellyfish as a potentially successful invader in the scenario of a warming Mediterranean Sea.

Aquaculture facilities promote populational stability throughout seasons and increase medusae size for the invasive jellyfish Cassiopea andromeda.

Cassiopea jellyfish have successfully invaded several marine ecosystems worldwide. We investigated if Cassiopea andromeda grows larger (umbrella size) and if their populations are more stable in shrimp farms than in mangroves in the Brazilian coast. Our results show that jellyfish abundance is higher in the shrimp farm during the rainy season and in the mangrove during dry season. The population is stable during both seasons in the shrimp farm, but unstable in the mangroves, as jellyfish are absent during rainy season. Shrimp farm-associated jellyfish are three times larger than those in the mangroves, regardless of season. We recorded the largest (49.2 cm of umbrella diameter) ever C. andromeda individual in the shrimp farm. Unlike the mangroves, the shrimp farm provides environmental intra-annual stability that promotes jellyfish growth and population persistence. Therefore, C. andromeda populations can be seasonally dynamic and artificial environments such as aquaculture facilities may facilitate the invasion process.