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Symbiont Identity Influences Patterns of Symbiosis Establishment, Host

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Symbiont Identity Influences Patterns of Symbiosis Establishment, Host Reference: Biol. Bull. 234: 1–10. (February 2018) © 2018 The University of Chicago Symbiont Identity Influences Patterns of Symbiosis Establishment, Host Growth, and Asexual Reproduction in a Model Cnidarian- Dinoflagellate Symbiosis YASMIN GABAY1, VIRGINIA M. WEIS2, AND SIMON K. DAVY1,* 1School of Biological Sciences, Victoria University of Wellington, Kelburn Parade, Wellington 6140, New Zealand; and 2Department of Integrative Biology, Oregon State University, Corvallis, Oregon 97331 Abstract. The genus Symbiodinium is physiologically di- study enhances our understanding of the link between symbi- verse and so may differentially influence symbiosis establish- ont identity and the performance of the overall symbiosis, ment and function. To explore this, we inoculated aposymbiotic which is important for understanding the potential establish- individuals of the sea anemone Exaiptasia pallida (commonly ment and persistence of novel host-symbiont pairings. Impor- referred to as “Aiptasia”), a model for coral symbiosis, with one tantly, we also provide a baseline for further studies on this of five Symbiodinium species or types (S. microadriaticum, topic with the globally adopted “Aiptasia” model system. S. minutum, phylotype C3, S. trenchii,orS. voratum). The spatial pattern of colonization was monitored over time via Introduction confocal microscopy, and various physiological parameters were Among the most significant marine mutualisms are those measured to assess symbiosis functionality. Anemones rapidly between cnidarians and their photosynthetic dinoflagellate formed a symbiosis with the homologous symbiont, S. minu- symbionts (Roth, 2014). These interactions, in particular, be- tum, but struggled or failed to form a long-lasting symbiosis tween anthozoan cnidarians (e.g., corals and sea anemones) with Symbiodinium C3 or S. voratum, respectively. Symbio- and dinoflagellates of the genus Symbiodinium, underpin the dinium microadriaticum and S. trenchii were successful but existence and success of coral reef ecosystems (Little et al., reached their peak density two weeks after S. minutum. The 2004; Wang et al., 2012; Lesser et al., 2013). spatial pattern of colonization was identical for all Symbio- The genus Symbiodinium is very diverse, consisting of nine dinium taxa that were ultimately successful, starting in the oral clades (A–I) and numerous subclades (types) and species (La- disk and progressing to the tentacles, before invading the col- Jeunesse, 2002; Pochon and Gates, 2010) that display consid- umn and, finally, the pedal disk. In all cases, proliferation erable physiological diversity (Schoenberg and Trench, 1980a; through the anemone’s tentacles was patchy, suggesting that Fitt et al., 1981; Chang et al., 1983; Iglesias-Prieto et al.,2004; symbionts were being expelled into the gastrovascular cavity Robison and Warner, 2006; Hennige et al., 2009). Given this, and re-phagocytosed by the host. However, the timing of these different symbiont taxa can differentially affect host and, hence, various spatial events differed between the different Symbio- holobiont (i.e., the entire symbiotic entity) performance. For dinium taxa. Furthermore, S. microadriaticum and S. trenchii example, in corals, some members of clades A and D can be were less beneficial to the host, as indicated by lower rates of less beneficial to their hosts than members of clade C, with photosynthesis, anemone growth, and pedal laceration. This lower rates of photosynthetic carbon fixation and translocation Received 8 September 2017; Accepted 7 December 2017; Published to the host and reduced host fitness (Mieog et al., 2009; Leal online 21 March 2018. et al., 2015). Alongside host phylotype and the prevailing en- * To whom correspondence should be addressed. E-mail: simon.davy@ vironmental conditions, symbiont identity may therefore de- vuw.ac.nz. Abbreviations: DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; P∶R, termine the fate of the symbiosis (Loram et al., 2007; Yuyama ratio of hourly gross photosynthesis to respiration. et al., 2016). 1 This content downloaded from 128.193.154.084 on June 06, 2018 13:21:51 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 2 Y. GABAY ET AL. Such observations have led to the proposal that several Sym- grown in the lab at 25 7C and an irradiance of 100 lmol pho- biodinium taxa might exhibit more opportunistic, and even tons m22 s21 (light/dark cycle of 12 h∶12 h) and fed twice parasitic, traits than others (Stat and Gates, 2011; Lesser et al., weekly with freshly hatched Artemia nauplii. To generate apo- 2013; Pettay et al., 2015; Silverstein et al., 2015). Starzak symbiotic (i.e., symbiont-free) anemones, animals were in- et al. (2014) tested this idea more broadly by modeling carbon cubated in a solution of 0.27 mmol l21 menthol in filtered sea- fluxes in the model symbiotic anemone Aiptasia when colo- water (FSW; 0.22 mm-FSW)for8h,afterwhichthementhol nized by a range of different Symbiodinium taxa. These mod- in FSW was removed and the anemones were incubated in els suggested that the usual homologous symbiont (S. minu- 5 mmol l21 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) tum, internal transcribed spacer region 2 [ITS2] type B1) in FSW overnight, as described by Matthews et al. (2015). forms a more beneficial symbiosis with Aiptasia than do sev- The treatment was repeated daily for four weeks or until no eral nonnative heterologous symbiont types, such as A1.4, E, symbionts were present, as determined by confocal micros- and F5.2; Symbiodinium E and F5.2 were, on occasion, even copy (IX81, Olympus, Auckland, New Zealand; 635 nm laser, observed to cause host mortality (Starzak et al.,2014).How- 655–755-nm emission filter). ever, direct measures of host growth and reproductive output, Cultured Symbiodinium from five clades were used as in- to corroborate the models of Starzak and coworkers, have not oculates (Table 1). Species names of these dinoflagellates are been performed. Indeed, we still know relatively little about used where available; otherwise, the ITS2 type is given. The al- the behavior and physiology of homologous and heterologous gae were subcultured from long-term (>5 y) laboratory stocks Symbiodinium taxa, in general, during symbiosis establishment, and grown in silica-free f/2 medium (Sigma-Aldrich, Auck- including whether they exhibit similar spatial patterns of uptake land, New Zealand) at 25 7C and an irradiance of 100 mmol and host colonization. Such information is important for under- photons m22 s21 on a light/dark cycle of 12 h∶12 h. All cul- standing the events that might occur during the establishment of tures were sampled for experimental use during the log phase novel host-symbiont pairings, such as after a coral bleaching of growth. event. Furthermore, such details are important for understand- ing the drivers of host-symbiont specificity, that is, the reasons Inoculation of aposymbiotic anemones with symbionts why many hosts are found in association with only one or a Following 1 wk of starvation, a total of 312 aposymbiotic few Symbiodinium taxa and vice versa (Baker, 2003; LaJeu- anemones (n 5 60 anemones for each Symbiodinium type nesse et al., 2004; Coffroth et al., 2010). and/or species; n 5 12 uninoculated anemones as a negative This study addressed these knowledge gaps using the sea control) of similar size (2–3-mm oral disk diameter) were anemone Exaiptasia pallida (Agassiz in Verrill, 1864), com- transferred to 400-ml clear plastic jars (one anemone per monly referred to as “Aiptasia,” a widely adopted model sys- jar) filled with FSW and allowed to settle for 3 days. Each al- tem for the study of reef-building corals and the cnidarian- gal culture was diluted in 25 ml FSW and 1 drop of Artemia dinoflagellate symbiosis (Weis et al., 2008; Baumgarten et al., nauplii suspension added, to give a final concentration of ~1 Â 2015). The current study measured the influence of symbiont 2 106 cells ml 1. The anemones were inoculated with one of the diversity on host colonization dynamics, as well as host per- five different symbiont cultures by pipetting with a glass pi- formance. We employed five different Symbiodinium species pette 1 ml of this dinoflagellate suspension onto the oral disk or types, representing a wide range of clades (A–E) and phys- of each anemone. Colonization was then monitored over a iologies, including the free-living and relatively heterotrophic period of 8 weeks, with sampling at 1, 2, 4, 6, and 8 weeks S. voratum (type E; Jeong et al., 2012) and the thermally tol- after inoculation. During this time, the anemones were fed erant but opportunistic S. trenchii (type D1a; Pettay and Lajeu- twice weekly with Artemia nauplii, with each feeding fol- nesse, 2009). Specifically, we asked whether symbiont iden- lowed by a water change. Seawater temperature was main- tity affects (1) symbiont cell proliferation, (2) colonization tained at 25 7C in a controlled-temperature room, and irradi- pattern inside the host, (3) photosynthetic performance, and 2 2 ance was held at ~100 mmol photons m 2 s 1 on a light/dark (4) host fitness. In doing so, we provide not only further in- cycle of 12 h∶12 h. sight into the cellular events that occur during host coloniza- tion by symbiotic dinoflagellates and the physiological impli- Symbiont proliferation cations of symbiont diversity but also a baseline from which to conduct more detailed studies of symbiosis establishment Spatial pattern of colonization. To determine the effect of and
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