Abstract
Cnidarian-dinoflagellate symbioses are ecologically important and the subject of much investigation. However, our understanding of critical aspects of symbiosis physiology, such as the partitioning of total respiration between the host and symbiont, remains incomplete. Specifically, we know little about how the relationship between host and symbiont respiration varies between different holobionts (host-symbiont combinations). We applied molecular and biochemical techniques to investigate aerobic respiratory capacity in naturally symbiotic Exaiptasia pallida sea anemones, alongside animals infected with either homologous ITS2-type A4 Symbiodinium or a heterologous isolate of Symbiodinium minutum (ITS2-type B1). In naturally symbiotic anemones, host, symbiont, and total holobiont mitochondrial citrate synthase (CS) enzyme activity, but not host mitochondrial copy number, were reliable predictors of holobiont respiration. There was a positive association between symbiont density and host CS specific activity (mg protein−1), and a negative correlation between host- and symbiont CS specific activities. Notably, partitioning of total CS activity between host and symbiont in this natural E. pallida population was significantly different to the host/symbiont biomass ratio. In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts. Furthermore, the relationship between the partitioning of total CS activity and the host/symbiont biomass ratio differed between holobionts. These data have broad implications for our understanding of cnidarian-algal symbiosis. Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host. The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.
Highlights
IntroductionSymbioses in which one partner (the symbiont) resides within the cells of a larger host organism to form a “holobiont” (used here as the host-symbiont unit) are widespread and contribute significantly to the success of some important biological groups (Douglas, 2010)
Symbioses in which one partner resides within the cells of a larger host organism to form a “holobiont” are widespread and contribute significantly to the success of some important biological groups (Douglas, 2010)
Our quantification of mitochondrial genome copy number as a predictor of mitochondrial density was less informative than we expected, but such an approach is worthy of more attention in a clonal population or in individuals undergoing stress
Summary
Symbioses in which one partner (the symbiont) resides within the cells of a larger host organism to form a “holobiont” (used here as the host-symbiont unit) are widespread and contribute significantly to the success of some important biological groups (Douglas, 2010). The second technique, known as the “growth rate method,” relies on measurements of light- and dark oxygen fluxes alongside estimations of in-hospite symbiont growth rates and carbon contents (usually inferred from mitotic indices and cell volumes, respectively) to estimate the contribution of zooxanthellae (=Symbiodinium) to animal respiration (commonly abbreviated as CZAR) (Muscatine et al, 1981, 1983; McCloskey and Muscatine, 1984) This method has been applied more widely than have the 14C or 13C methods, presumably due to the relative ease with which oxygen fluxes can be measured (Fitt et al, 1982; Muller-Parker, 1984; Muscatine et al, 1984; Steen and Muscatine, 1984; Davies, 1991; Davy et al, 1996; Verde and McCloskey, 1996; Fitt and Cook, 2001; Grottoli et al, 2006; Starzak et al, 2014). These approaches are not satisfactory, since the first assumes no effect of symbiont density on host respiration, and the second is likely confounded by the respiratory activities of residual host material and substantial physiological changes when Symbiodinium are removed from the host (see Goiran et al, 1996, 1997; Wang et al, 2011)
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