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Together Is Better: the Importance of Heterotrophy and Photoautotrophic

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Together Is Better: the Importance of Heterotrophy and Photoautotrophic Explorations |Biological Sciences Together is Better: The Importance of Heterotrophy and Photoautotrophic Symbiosis for Growth of the Sea Anemone Aiptasia pallida Jack Cushman Koch University of North Carolina Wilmington Faculty Mentor: Joe Pawlik University of North Carolina Wilmington ABSTRACT Scleractinian corals are important because they are the foundation species that build coral reefs, but they are in decline worldwide. The sea anemone Aiptasia pallida is a possible model system for studying the nutrition of reef-building corals because both have the same algal symbionts (Symbiodinium spp.). The relative importance of exogenous nutrition (NX) versus symbiont-derived nutrition (Ns) for A. pallida is largely unknown. When stressed, both anemo- nes and corals bleach (expel symbionts) and have to rely solely on NX. I measured changes in wet mass after 60 days for anemones divided into four treatments that manipulated the presence and absence of NX and Ns. The treatments were: symbionts present and food provided (S+/F+), symbionts absent, but food provided (S-/F+), symbionts present, but no food provided (S+/F-), and neither symbionts present nor food provided (S-/F-). TetraMin fake food was used for ex- ogenous food. Anemones were rendered aposymbiotic using a combination of cold shocks and treatments with a photosynthesis-inhibiting compound, and subsequently maintained in dark- ness. Anemones with S+/F+ gained signifcantly more mass than other treatments (p<0.001). All other treatments lost mass and there were no signifcant differences among them. Under the experimental conditions used in this study, A. pallida needed both NX and Ns to grow, sug- gesting that some component of each nutritional source is necessary for the health of this sea anemone. ymbiotic relationships are ubiquitous in 1.1 Symbiosis Snature and can be classifed into three sub-categories: mutualism, parasitism, and Symbiotic relationships often involve ad- commensalism. These sub-categories are aptations that enable the success of the asso- complex and many change over time on a ciation (Furla et al., 2005). In cnidarian (e.g. continuum from parasitism to mutualism de- corals, jellyfsh, and sea anemones) symbi- pending on environmental conditions, and otic relationships with algae, the association possible interactions among host and sym- can be facultative or obligate and usually biont genotypes (Muller-Parker et al., 1990; consists of the transfer of nutritionally use- Neuhauser & Fargione, 2004; Thrall et al., ful compounds (photosynthetically-derived 2007; Lesser et al., 2013). carbon and metabolic waste products) from 46 Jack Koch one partner to the other (Muller-Parker & bleaching include increased light intensity, Davy, 2001; Buhl-Mortensen & Mortensen, decreased pH, changes in seawater tempera- 2004; Burriesci et al., 2012). The stability of ture and chemistry, and pollution. However, symbiotic relationships between cnidarians the conditions under which bleaching occurs and their algal symbionts are under threat is a species-specifc phenomenon (Gates et by anthropogenic and climate-related factors al., 1992; Edmunds, 1994; Fitt et al., 2001). (Hoegh-Guldberg et al., 2007; Lesser et al., In some cases, bleaching may lead to death of 2013). Global climate change (e.g., changes the host due to starvation, although in other in sea surface temperature and ocean acidi- cases, recovery of the host is possible through fcation), disease, and other negative infu- increased heterotrophic feeding or reinfec- ences (e.g., pollution and sedimentation) tion with symbionts (Steen, 1987; McAuley may cause the host to expel its symbionts & Cook, 1994; Anthony & Fabricius, 2000; (Burriesci et al., 2012). Fitt & Cook, 2001; Knowlton, 2001; Borell Reef-building coral symbioses are the et al., 2008). Coral growth, and therefore reef best-known example of marine symbioses formation, is dependent upon nutrition pro- and contribute to the importance of coral vided by zooxanthellae (Muscatine, 1967; reefs in global marine health and to the abil- Muscatine & Cernichiare, 1969; Burriesci et ity of coral reefs to provide a range of eco- al., 2012; Lehnert et al., 2014). logical services. These services include food, After a bleaching event, the host must fnd recreation, coastal protection, habitat, and additional sources of exogenous nutrition nutrient cycling (Moberg & Folke, 1999). (NX) to compensate for the loss of symbiont- Unfortunately, corals are diffcult to study derived nutrition (Ns). Anemones such as in the lab because they grow and reproduce Anthopleura elegantissima and Aiptasia pal- slowly and they have an endoskeleton. The lida have the ability to derive 100% of their calcareous endoskeleton makes it diffcult daily nutritional needs from NX and use the to measure their tissue mass and even more symbiotic association to compensate for the diffcult to maintain the animal, because of ATP required to capture food (Engebretson the requirements for very specifc seawater & Muller-Parker, 1999; Bergschneider & chemistry (Lehnert et al., 2012). In addition, Muller-Parker, 2008; Weis et al., 2008; regulations restricting coral collection and Lehnert et al., 2012). Other organisms, like manipulation make it diffcult to study cor- corals, can increase heterotrophic feeding als in the laboratory and feld (Lehnert et al., efforts when Ns is inadequate (Anthony & 2012). Fabricius, 2000; Ferrier-Pagès et al., 2010; Hoogenboom et al., 2010). 1.2 The Bleaching Response 1.3 The Sea Anemone Aiptasia and The The cnidarian-zooxanthellae symbi- Dinofagellate Symbiodinium otic relationship undergoes a phenomenon called bleaching (Davy et al., 2012). This Sea anemone species in the genus Aiptasia phenomenon is becoming more prevalent are found worldwide in temperate and tropi- on coral reefs world-wide as environmen- cal waters (Sunagawa et al., 2009; Leal et tal conditions become increasingly stressful al., 2012). The temperate species A. pallida (Hoegh-Guldberg, 1999). Bleaching is the (Agassiz in Verrill, 1864) and Symbiodinium process in which corals eject their symbionts (see Figure 1) engage in a symbiosis that is or their symbionts cease to synthesize their similar to corals and their Symbiodinium. photosynthetic pigments due to environmen- A. pallida are mixotrophs, feeding on mi- tal, chemical, or physical stressors (Gates croplankton from the water column and re- et al., 1992; Brown & Ogden, 1993; Glynn, ceiving photosynthate from Symbiodinium 1996; Weis et al., 2008). Factors that cause (Muscatine, 1967; Muscatine & Cernichiare, 47 Explorations |Biological Sciences Figure 1. Tentacle squash from temperate symbiotic sea anemone Anthopleura elegantissima at 40x power oil immersion under differential interference contrast microscope. Symbiodinium are the golden-brown circles. Although this is not the genus of sea anemone in this study, the Symbiodinium are similar. Dinofagellate species assigned to Symbiodinium are found world- wide in temperate and tropical waters as both endosymbionts and as free-living microalgae (Lajeunesse & Trench, 2000). The dominant vegetative form is a single, spherical or broadly ellipsoidal pigmented cell ranging from 5 – 15 µm in diameter (Freudenthal, 1962). A motile phase is present, but only when the alga is free-living. Scale bar is 10 µm. 1969; Muscatine, 1980a; Burriesci et al., 1.4 The Symbiotic Relationship Between 2012). Compared to most corals, A. pallida Aiptasia and Symbiodinium survives under a wider array of conditions in the lab and feld, grows and reproduces rap- The symbiosis between cnidarians and idly, and is easy to collect and manipulate, Symbiodinium is highly specifc. Anemones, making this anemone and its symbionts an for example, may initially take up many ideal model system for studying the ecology clades of Symbiodinium, but preferential and physiology of reef-building corals (Weis clades outcompete others over time (Belda- et al., 2008). Baillie et al., 2002). Even when there is The relationship between A. pallida and not competition among clades within hosts, Symbiodinium boosts the overall ftness of the some anemones are unable to host particular anemone when compared to aposymbiotic in- Symbiodinium clades; this incompatibility is dividuals (Fitt & Pardy, 1981). Previous stud- reportedly caused by the inability of the host ies indicate that starved symbiotic A. pallida and symbiont to recognize each other (Belda- use zooxanthellae-derived photosynthate to Baillie et al., 2002). The symbiosis between fulfll their daily nutritional needs whereas A. pallida and Symbiodinium is facultative starved aposymbiotic anemones use host- and not required for the survival of the host. derived lipids to fulfll their daily nutritional Symbionts inhabit a host-derived vacuole needs (Muscatine, 1961; Fitt & Pardy, 1981). called a symbiosome that is located within Reliance on host-derived lipids contributes to gastrodermal cells of the host (Wakefeld et an increased rate of mass loss when compared al., 2000; Kazandjian et al., 2008). The sym- to starved symbiotic anemones (Muscatine, biosome protects the algal cell and enables 1961; Fitt & Pardy, 1981). the transfer of inorganic nutrients from host 48 Jack Koch to symbiont and organic nutrition from sym- nutritional needs of the anemone. The anem- biont to host (Rahav et al., 1989; Cook et al., ones with neither symbionts present nor food 1992; Yellowlees et al., 2008; Davy et al., provided (S-/F-) would lose the most mass; 2012; Detournay et al., 2012). The host de- this treatment
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