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Soft Coral Sarcophyton (Cnidaria: Anthozoa: Octocorallia) Species Diversity and Chemotypes

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Soft Coral Sarcophyton (Cnidaria: Anthozoa: Octocorallia) Species Diversity and Chemotypes Soft Coral Sarcophyton (Cnidaria: Anthozoa: Octocorallia) Species Diversity and Chemotypes Satoe Aratake1, Tomohiko Tomura1, Seikoh Saitoh2, Ryouma Yokokura3, Yuichi Kawanishi2, Ryuichi Shinjo4, James Davis Reimer5, Junichi Tanaka3, Hideaki Maekawa2* 1 Graduate School of Science and Engineering, University of the Ryukyus, Nishihara, Okinawa, Japan, 2 Center of Molecular Biosciences, Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan, 3 Department of Chemistry, Biology, and Marine Science, University of the Ryukyus, Nishihara, Okinawa, Japan, 4 Department of Physics and Earth Sciences, University of the Ryukyus, Nishihara, Okinawa, Japan, 5 Rising Star Program, TRO-SIS, University of the Ryukyus, Nishihara, Okinawa, Japan Abstract Research on the soft coral genus Sarcophyton extends over a wide range of fields, including marine natural products and the isolation of a number of cembranoid diterpenes. However, it is still unknown how soft corals produce this diverse array of metabolites, and the relationship between soft coral diversity and cembranoid diterpene production is not clear. In order to understand this relationship, we examined Sarcophyton specimens from Okinawa, Japan, by utilizing three methods: morphological examination of sclerites, chemotype identification, and phylogenetic examination of both Sarcophyton (utilizing mitochondrial protein-coding genes MutS homolog: msh1) and their endosymbiotic Symbiodinium spp. (utilizing nuclear internal transcribed spacer of ribosomal DNA: ITS- rDNA). Chemotypes, molecular phylogenetic clades, and sclerites of Sarcophyton trocheliophorum specimens formed a clear and distinct group, but the relationships between chemotypes, molecular phylogenetic clade types and sclerites of the most common species, Sarcophyton glaucum, was not clear. S. glaucum was divided into four clades. A characteristic chemotype was observed within one phylogenetic clade of S. glaucum. Identities of symbiotic algae Symbiodinium spp. had no apparent relation to chemotypes of Sarcophyton spp. This study demonstrates that the complex results observed for S. glaucum are due to the incomplete and complex taxonomy of this species group. Our novel method of identification should help contribute to classification and taxonomic reassessment of this diverse soft coral genus. Citation: Aratake S, Tomura T, Saitoh S, Yokokura R, Kawanishi Y, et al. (2012) Soft Coral Sarcophyton (Cnidaria: Anthozoa: Octocorallia) Species Diversity and Chemotypes. PLoS ONE 7(1): e30410. doi:10.1371/journal.pone.0030410 Editor: Dirk Steinke, Biodiversity Insitute of Ontario - University of Guelph, Canada Received September 8, 2011; Accepted December 15, 2011; Published January 17, 2012 Copyright: ß 2012 Aratake et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The project of ‘‘Research of insertion mechanism into the genome of movable gene with its transporter and development of the general gene introduction system’’ was supported by Ministry of Education, Culture, Sports, Science and Technology Japan. International Research Hub Project for Climate Change and Coral Reef/Island Dynamics, University of the Ryukyus. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction revised the classification of Sarcophyton after gross morphological and microscopic examination of Sarcophyton species’ type speci- Soft corals (Cnidaria: Anthozoa: Octocorallia) often equal or mens. Since the taxonomic revision by Verseveldt [7], who exceed the total coverage of scleractinian corals in coral reef considered Sarcophyton to contain 35 valid species, an additional six ecosystems [1–4], and as dominant space-occupiers, important species of Sarcophyton have been described [8–13]. structural components of coral reef communities, and contributors Recently, McFadden et al. [14] reported on the utility of to coral reef biomass [4,5], have been the subjects of biological mitochondrial protein-coding gene MutS homolog (msh1) sequenc- studies since the nineteenth century. es for Sarcophyton and Lobophytum species identification. The study The subclass Octocorallia includes soft corals, gorgonians, and sea showed that within Sarcophyton, specimens initially identified as pens. Most soft corals belong to the order Alcyonacea, which is Sarcophyton glaucum by morphology could be divided into six very comprised of the families Xeniidae, Nephtheidae, and Alcyoniidae. distinct genetic clades, suggesting that this morphologically The family Alcyoniidae contains the genera Sinularia, Lobophytum and heterogeneous species is actually a complex of cryptic species [14]. Sarcophyton, and members of this group are among the dominant The soft coral genera Lobophytum and Sarcophyton are known to benthic organisms in the coral reefs in Okinawa and other Pacific have many secondary metabolites [15–17]. Secondary metabolites Ocean areas [1,2,4,6]. Sarcophyton species are very hardy and are in soft corals of Sarcophyton have been well characterized with the dominant in many coral reef areas. Sarcophyton species are character- advancement of instrumental analyses over the past four decades. ized by a distinct sterile stalk, a broad, flared, smooth, mushroom- The soft coral egg-specific secondary metabolite PGA2 and some shaped top called a capitulum, and by the shape of their sclerites, diterpenes have been shown to cause contractions of soft coral which are found in the interior coenenchymal tissue of the colony. polyps and the expulsion of eggs during spawning [18], and similar Most soft coral classification and identification has traditionally phenomenon by a secondary metabolite (sarcophytoxide) has been been carried out by sclerite characterization. Verseveldt [7] reported from Sarcophyton glaucum [19]. These examples indicate PLoS ONE | www.plosone.org 1 January 2012 | Volume 7 | Issue 1 | e30410 Chemotype Diversity of Sarcophyton one reproductive isolation factor may be due to chemical signals, F [14], and specimens from this study belonged to four of these and that secondary metabolites may have important function. In clades: four sequences within clade B sensu McFadden et al. [14], addition, some metabolites are toxic and used in competition for one within C, five within D, and six within F. space with scleractinian corals [20], and it is believed that octocorals release chemical substances into the water as a Major compound analyses: Cembrene diterpenes commonly used strategy to inhibit growth and survival of their In total eight cembranoid diterpenes were identified (chemo- neighbors [21]. Furthermore, it is known in Sarcophyton glaucum that types 1–8) (Fig. 2). The abundance of each chemotype at each secondary metabolites such as sarcophytoxide cause allelopathic collection site is shown in Table 1. Among the detected effects [19]. Thus, by focusing attention on secondary metabolites chemotypes, 20 specimens of chemotype 1 (2S,7S,8S-sarcophyt- it may be possible to better understand the environmental role of oxide) were most abundant, followed by chemotype 2 (2S,7R,8R- soft corals in tropical waters. sarcophytoxide) and chemotype 3 (2S,7R,8R-isosarcophytoxide). One molecule, sarcophytol A, has attracted attention due to its The cembrenes found from the 34 specimens were as follows: antitumor promoting activity [22]. As sarcophytol A was discovered chemotype 1 - 2S,7S,8S-sarcophytoxide, 20 specimens (Sunabe 1, from Sarcophyton collected at Ishigaki Island, Okinawa, southern 5, 7, 10, 12, 13, 14, 15, 16, 18, 20, 21, 22, 23, Zanpa 1, 5, 9, Japan, researchers have investigated the chemical activity and three- Mizugama 6, 8, 11); chemotype 2 - 2S,7R,8R-sarcophytoxide, six dimensional structure of the chemical [23–25]. Additionally, Koh et specimens (Sunabe 1, 2, 5, 16, 17, Mizugama 7); chemotype 3 - al. [26] investigated the distribution of Sarcophyton species containing 2S,7R,8R-isosarcophytoxide, three specimens (Sunabe 6, 19, sarcophytol A in Okinawa, and their study indicated that Mizugama 4); chemotype 4–7,8-epoxy-1,3,11-cembratrien-15-ol, composition of cembranoids in Sarcophyton is not related with one specimen (Sunabe 1); chemotype 5 - Sarcophytol A, one morphologically identified species. Subsequently, it was found that specimen (Mizugama 4); chemotype 6 - Emblide, two specimens two species, Sarcophyton trocheliophorum and Sarcophyton crassocaule, (Zampa 6, 10); chemotype 7 - 7-hydroxy-1,3,11-cembratrien-20,8- appeared to be the source organisms of sarcophytol A [27], and not olide, two specimens (Zampa 3, 4); chemotype 8 - 7S,8S-epoxy- only Sarcophyton glaucum as originally reported. During this study, it 1,3,11-cembratriene (Sunabe 10). was also noted that Sarcophyton glaucum’s chemical content varied to a All specimens of Sarcophyton trocheliophorum included the same large degree and it was concluded there are at least nine chemotypes chemotype, chemotype 1. Specimens of Sarcophyton glaucum clade F within S. glaucum [27]. included two chemotypes, 6 and 7. Chemotypes 6 and 7 have Thus, it is difficult to conclusively identify the source Sarcophyton lactone function and could be easily distinguished from the other species of secondary
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