Symbiont carbon and nitrogen assimilation in the Cassiopea–Symbiodinium mutualism

Abstract

Symbiotic interactions in the marine environment have long been represented by mutualisms between photosymbionts and benthic marine invertebrates like corals and sponges. Although 'upside-down' epibenthic jellyfish in the genus Cassiopea also derive a substantial metabolic benefit from abundant communities of the dinoflagellate symbiont Symbiodinium, comparatively little is known about the efficiency of carbon (C) and nitrogen (N) assimilation within the Cassiopea holobiont. Using standardized 6 h incubations with 13 C-and 15 N-enriched compounds, we assessed symbiont C and N assimilation in both oral arm and bell tissue of C. xamachana under light and dark conditions. Carbon fixation was light dependent and highest in the photosymbiont-rich oral arm tissue. In contrast, 15 NO 3 assimilation was light independent in both tissue types and was highest in bell tissue that was sparsely colonized by photosymbionts. This, coupled with higher bell tissue 15 N enrichment under dark conditions, implicates nonphotosynthetic microbes in Cassiopea N metabolism. This zonation of microbial activity may allow C. xamachana to simultaneously fix C and assimilate ambient or porewater N released during Cassiopea pumping activity. Although C. xamachana may utilize symbiont-derived N, lower 15 N enrichment relative to C fixation suggests that Cassiopea may also rely on exogenous sources of N for growth. This study provides initial evidence that the efficiency of symbiont metabolism within Cassiopea jellyfish is comparable to, or exceeds, that of other common benthic marine invertebrates, sup porting the contention that Cassiopea have an important role in the productivity and nutrient dynamics within their local environment.

Upside-Down but Headed in the Right Direction: Review of the Highly Versatile Cassiopea xamachana System

“…These experiments showed that labeled glycerol disappeared in <30 min, likely through utilization in lipid synthesis, as suggested by the authors; these findings were later corroborated with findings of a similar study on the sea anemone Exaiptasia (Davy and Cook, 2001). In vivo carbon fixation by the symbiont is highly efficient in C. xamachana, with rates exceeding daily respiration requirements of the host, supporting a growth rate of 3% body weight per day (Verde and McCloskey, 1998;Welsh et al, 2009;Freeman et al, 2016). Contrary to carbon, nitrogen assimilation levels under both photosynthetic and non-photosynthetic conditions are low, suggesting alternative nitrogen sources are essential for life.…”

“…High light penetrance is important for species within this genus, as the jellyfish hosts one or more photosynthetic dinoflagellate species of the genus Symbiodinium (Hofmann et al, 1996;Lampert, 2016). Similar to their coral relatives, nutrient exchange is a key component supporting this cnidarian-dinoflagellate mutualism (Hofmann and Kremer, 1981;Welsh et al, 2009;Freeman et al, 2016). In addition, Cassiopea spp.…”

Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses

“…Cyanobacteria are mostly associated with marine sponges and diatoms (see reviews by Freeman & Thacker, 2011;Foster et al, 2011;Venn et al, 2008), although they are also symbionts of haptophytes or dinoflagellates . Overall, for all these photosynthetic symbioses, light is of prime importance because it is needed by the symbionts as an energy source to fix inorganic carbon into organic compounds called photosynthates, most of which are transferred to the host for its own use (Freeman et al, 2016). Algae, such as dinoflagellates of the genus Symbiodinium, are associated with benthic animals such as reef-building corals, sea anemones, tridacnid molluscs, jellyfish (Cassiopea sp.…”

“…Algae, such as dinoflagellates of the genus Symbiodinium, are associated with benthic animals such as reef-building corals, sea anemones, tridacnid molluscs, jellyfish (Cassiopea sp. ), and foraminifera (Freeman, Stoner, Easson, Matterson, & Baker, 2016;Sachs & Wilcox, 2006;Venn et al, 2008). In the pelagic environment, photosymbiotic interactions also exist between microalgae and other protists (radiolarian, foraminifera) or metazoans (ciliates, dinoflagellates), although the exact nature of this partnership is often not formally demonstrated.…”

“…In the pelagic environment, photosymbiotic interactions also exist between microalgae and other protists (radiolarian, foraminifera) or metazoans (ciliates, dinoflagellates), although the exact nature of this partnership is often not formally demonstrated. Overall, for all these photosynthetic symbioses, light is of prime importance because it is needed by the symbionts as an energy source to fix inorganic carbon into organic compounds called photosynthates, most of which are transferred to the host for its own use (Freeman et al, 2016). In addition, algal symbionts play a major role in the acquisition of inorganic nitrogen (ammonium, nitrate), phosphorus, and other macro-and micronutrients essential for the symbiosis (Tanaka, Miyajima, & Koike, 2006).…”