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Identification of Photosynthetic Sacoglossan Species

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Identification of Photosynthetic Sacoglossan Species 112 Encocytobiosis Cell Res. (2009) 19, 112-119 Identification of photosynthetic sacoglossans from Japan Yoshiharu Y. Yamamoto1,2, Yoichi Yusa3, Shoko Yamamoto3, Yayoi Hirano4, Yoshiaki Hirano4, Taizo Motomura5, Takanori Tanemura1, Junichi Obokata1,6,* 1Center for Gene Research, Nagoya University, Nagoya 464-8602, Japan; 2Faculty of Applied Biological Sciences, Gifu University, Yanagido 1-1, Gifu City, 501-1193, Japan; 3Department of Biological Sciences, Faculty of Science, Nara Women’s University, Kitauoyanishi, Nara, Nara 630-8506, Japan; 4Department of Biology, Faculty of Science, Chiba University, Yayoi-cho, Inage-ku, Chiba, Chiba 263-8522, Japan; 5Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran 051-0003; 6Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto 606-8552, Japan. * Corresponding author: [email protected], [email protected] Abstract days to months, depending on species. This Some sacoglossan molluscs, including several incorporation and maintenance is called as species of Elysiidae, are known to incorporate kleptoplasty (TRENCH and OHLHORST 1976; algal chloroplasts, and the incorporated chlo- RUMPHO et al. 2007). roplasts are functional for days to months, After the first report of kleptoplasty by Elysia depending on species. This incorporation and astroviridis (KAWAGUTI and YAMASU 1965), maintenance of foreign chloroplasts are known several species have been shown to have as kleptoplasty. In this article, we surveyed kleptoplasts by transmission electron micro- photosynthetic activity of several sacoglos- scopic (TEM) analysis (TRENCH et al. 1969). sans collected in Japan, by analysis of in vivo Functionality of kleptoplasts was demon- chlorophyll fluorescence. Our survey found 8 strated by light-driven CO2-incorporation using new species that have active chlorophylls, radioisotope (14C) (HINDE and SMITH 1974), judged by the parameter Fv/Fm, an indicative light-dependent O2-emission detected by of the functionality of photosystem II. Identified oxygen electrode (RUMPHO et al. 2000), and in sacoglossans with active chlorophylls belong vivo chlorophyll fluorescence analysis for de- to the Bosella, Costasiella, Elysia, Julia, tection of functional chlorophylls (EVERTSEN et Placida, Stiliger, and Thuridilla genera. Our al. 2007). Now, kleptoplasts have been found results strongly suggest that these species in more than 20 species of sacoglossans that possess kleptoplasts. Possession of chloro- belong to genera Alderia, Bosellia, Caliphylla, plasts was confirmed for one of the identified Elysia, Hermaea, Limapontia, Mourgona, sacoglossans, Elysia trisinuata, by transmis- Oxynoe, Plakobranchus, Tridachia, and sion electron microscopy. Thuridilla (EVERTSEN et al. 2007). In this report, we screened for Japanese Introduction sacoglossans containing functional chloro- Some sacoglossans are known to have ability plasts, judged by possession of active chlo- to photosynthesize using chloroplasts present rophylls that can be detected by in vivo chlo- in their cells. These chloroplasts are not inher- rophyll fluorescence analysis. We first report ited from the parents, but “stolen” from their possession of active chlorophylls in eight spe- food algae, such as Codium or Caulerpa. Ac- cies, including ones belonging to Costasiella, quired algal chloroplasts are maintained in Julia, Placida, and Stiliger genera. Our results, cells of digestive glands of sacoglossans for together with previous studies in this field, Yamamoto et al. – Identification of photosynthetic sacoglossans from Japan 113 suggest that kleptoplasty occur in a wide range 1963), and observed with a JEM-1011 electron of sacoglossans. microscope (JEOL, Tokyo, Japan). Materials and Methods Results and Discussions Sea slugs were collected in 2007 and 2008 at Sacoglossans collected at several shores in Kominato (Kamogawa, Chiba, Japan), Misaki Japan were subjected to in vivo chlorophyll (Miura, Kanagawa, Japan), Shirahama (Ni- fluorescence analysis. Plakobranchus ocella- shimuro, Wakayama, Japan), Sesoko (Motobu, tus and Pteraeolidia ianthina were used as Okinawa (Ryukyu), Japan), and Zanpa (Yomi- positive controls. P. o c ell a t u s has kleptoplasts tani-son, Okinawa, Japan). Collected sea (GREENE 1970b; HIROSE 2005), whose func- slugs were sent to Nagoya University and tionality has been confirmed by detection of subjected to in vivo chlorophyll fluorescence light-dependent CO2-fixation (GREENE 1970a) analysis using FluorCam (Photon Systems as well as Fv/Fm determined by in vivo chlo- Instruments, Brno, Czech Republic) based on rophyll fluorescence analysis (EVERTSEN et al. the pump and probe system with a CCD cam- 2007). P. ianthina is known to be a host of era detector (NEDBAL and WHITMARSH 2004). endosymbiotic zooxanthella, rather than klep- Fv/Fm (BAKER 2008) was measured per indi- toplasts. P. ianthina has also been reported to vidual using the camera system, and the av- have photosynthetic activity due to the sym- erage and standard deviation were calculated, bionts, revealed by light-dependent carbon if possible. Assays were done within a week fixation activity (HOEGH-GULDBERG and HINDE after collection except for Costasiella cf. ku- 1986). roshimae and Elysia ornata. These two spe- As shown in Table 1, both P. ocellatus and P. cies were assayed in a month after collection. ianthina showed high Fv/Fm, as expected. Until assays, E. ornata, Placida sp., and Co- These results confirmed possession of active stasiella cf. kuroshimae were kept together chlorophylls in these organisms. It should be with their food algae that are Codium, Codium, noted that this analysis cannot distinguish and Avrainvillea, respectively. Because we between kleptoplasts (P. ocellatus) and endo- could not prepare food algae for the other sea symbiotic algae (P. ianthina). slugs, it was impossible to adjust days before We collected 12 species in sacoglossa in assay after start of starvation. This problem Japan, and subjected them to in vivo chloro- caused some difficulty in strict comparison of phyll fluorescence analysis. Among them, 8 Fv/Fm among species. species showed measurable Fv/Fm values For transmission electron microscopy (TEM), (Table 1). These results indicate that the posi- samples were fixed with 3% glutaraldehyde in tive species, that belong to genera of Costa- 0.1 M cacodylate buffer (pH 7.2) containing siella, Bosellia, Elysia, Thuridilla, Julia, Placida, 3% NaCl for 2 h at 4˚C. In this fixative, the and Stiliger, possess active chlorophylls and samples were cut into small fragments. Then thus photosynthetically functional chloroplasts. they were postfixed with 1% OsO4 in 0.1 M Considering that all these species belong to cacodylate buffer (pH 7.2) containing 3% NaCl sacoglossa, these results strongly suggest that for 2 h at room temperature. They were dehy- they have kleptoplasts. Photographs of posi- drated with a graded acetone series and em- tive species are shown in Figure 1. bedded in Spurr’s epoxy resin. Thin sections One of the positive species, Elysia trisinuata, were cut by a diamond knife on a Ultracut was subjected to electron microscopic analysis (Reichert-Jung, Wien, Austria), mounted on (Figure 2). As expected, cells of digestive formvar-coated slot grids, stained with 4% glands contained chloroplasts (Ct in the Figure uranyl acetate and lead citrate (REYNOLDS 2B), judged by their ultrastructure. As shown in 114 Yamamoto et al. – Identification of photosynthetic sacoglossans from Japan Table 1: Sacoglossans with active chlorophylls identified in this study Number of Species Sampling place Sampling date Size (mm) Fv/Fm individuals SACOGLOSSA Costasiellidae Costasiella cf. ku- Zanpa 2008 Dec. 5 1-3 0.661 ± 0.0395 roshimae Elysiidae Bosellia sp. Sesoko 2008 Apr. 4 7-11 0.716 ± 0.052 Elysia ornata Shirahama 2007 Sep. 3 20-40 0.815 ± 0.0201 Ibid. Misaki 2007 Oct. 5 20-40 0.844 ± 0.0190 Elysia trisinuata Misaki 2007 Aug. 6 15-30 0.853 ± 0.042 Thuridilla vatae Sesoko 2008 Jun. 1 14 0.725 Juliidae Julia zebra Sesoko 2008 Apr. 1 2 0.616 Limapontiidae Placida sp. (sensu Sesoko 2008 Apr. 9 4 - 8 0.475 ± 0.075 (BABA 1986) Stiliger ornatus Shirahama 2008 Oct. 3 7-10 0.595 ± 0.0795 Plakobranchidae Plakobranchus ocel- Sesoko 2008 Jun. 1 22 0.811 latus NUDIBRANCHIA Pteraeolidia ianthina1 Kominato 2008 Oct. 4 20-50 0.831 ± 0.023 Kominato: Kamogawa, Chiba; Misaki: Miura, Kanagawa; Shirahama: Nishimuro, Wakayama; Sesoko: Motobu, Okinawa; Zanpa: Zanpamisaki, Yomitani-son, Okinawa. 1 Known to retain Symbiodinium by endosymbiosis (BURGHARDT et al. 2008). the figure, some chloroplasts possess starch Fv/Fm is a parameter that reflects maximum grains (white ovals, Figure 2B), suggesting efficiency of photosystem II, and thus it indi- functionality of these kleptoplasts. cates intactness of photosystem II (BAKER As shown in Table 1, Fv/Fm varies from 0.85 2008). Injury of photosystem II, that can be (Elysia trisinuata) to 0.48 (Placida sp.) ac- caused by environmental stresses, results in cording to species, and variation within a spe- reduction of Fv/Fm (BAKER 2008). Although cies was much smaller than difference among degree of injury against environmental species. As for Elysia ornata, we analyzed two stresses can vary among individuals, we found batches, one from Shirahama collected in that there is little variation of Fv/Fm among the September and the other from Misaki caught in analyzed individuals of the same species. October. Although these two groups were In the case of
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