Symbiont carbon and nitrogen assimilation in the Cassiopea–Symbiodinium mutualism

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 13Cand 15Nenriched 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, NO3 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 15N 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 15N 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.

[1]  N. Knowlton,et al.  Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses , 2015, The ISME Journal.

[2]  Cole G Easson,et al.  Shifts in sponge-microbe mutualisms across an experimental irradiance gradient , 2015 .

[3]  C. J. Freeman,et al.  Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras , 2014, PeerJ.

[4]  M. Fogel,et al.  Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades , 2013, The ISME Journal.

[5]  D. L. Alexander,et al.  Highly Dynamic Cellular-Level Response of Symbiotic Coral to a Sudden Increase in Environmental Nitrogen , 2013, mBio.

[6]  M. Fogel,et al.  Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? , 2013, The ISME Journal.

[7]  C. Layman,et al.  Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. , 2011, Marine pollution bulletin.

[8]  J. Weisz,et al.  Zooxanthellar Symbionts Shape Host Sponge Trophic Status Through Translocation of Carbon , 2010, The Biological Bulletin.

[9]  C. Wild,et al.  Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef , 2010 .

[10]  C. Wild,et al.  Organic matter release by the benthic upside-down jellyfish Cassiopea sp. fuels pelagic food webs in coral reefs , 2010 .

[11]  T. Meziane,et al.  Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production , 2009, Hydrobiologia.

[12]  E. Rosenberg,et al.  Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. , 2008, FEMS microbiology reviews.

[13]  R. Gates,et al.  Functional diversity in coral–dinoflagellate symbiosis , 2008, Proceedings of the National Academy of Sciences.

[14]  K. Pitt,et al.  Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production , 2008, Hydrobiologia.

[15]  N. Moran,et al.  Colloquium Papers: Symbiosis as an adaptive process and source of phenotypic complexity , 2007 .

[16]  G. Schmidt,et al.  Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium , 2006 .

[17]  B. Fry Stable Isotope Ecology , 2006 .

[18]  S. R. Santos,et al.  Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. , 2005, Protist.

[19]  A. Baker Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium , 2003 .

[20]  R. Henry,et al.  Localization and Quantification of Carbonic Anhydrase Activity in the Symbiotic Scyphozoan Cassiopea xamachana , 2003, The Biological Bulletin.

[21]  Todd C. LaJeunesse,et al.  Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs , 2002 .

[22]  C. Ferrier‐Pagès,et al.  Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations , 2002 .

[23]  L. R. McCloskey,et al.  Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season , 1998 .

[24]  P. Kremer,et al.  DIN, DON and P04 flux by a medusa with algal symbionts , 1992 .

[25]  L. Muscatine,et al.  Reef Corals: Mutualistic Symbioses Adapted to Nutrient-Poor Environments , 1977 .