Diversity of Free-Living Marine Ciliates (Alveolata, Ciliophora): Faunal
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Available online at www.sciencedirect.com ScienceDirect European Journal of Protistology 61 (2017) 424–438 Review Diversity of free-living marine ciliates (Alveolata, Ciliophora): Faunal studies in coastal waters of China during the years 2011–2016 a,b,1 a,c,h,1 a,d,1 a,e,1 a,1 Weiwei Liu , Jiamei Jiang , Yuan Xu , Xuming Pan , Zhishuai Qu , a,1 f g a,∗ a,c,∗ Xiaotian Luo , Hamed A. El-Serehy , Alan Warren , Honggang Ma , Hongbo Pan a Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China b Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou 510301, China c College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China d State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China e College of Life Science and Technology, Harbin Normal University, Harbin 150025, China f Department of Zoology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia g Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK h College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China Available online 21 April 2017 Abstract In the period 2011–2016, a series of investigations were carried out on the marine and brackish free-living ciliate fauna of the temperate–tropical coastal waters of China. About 210 morphotypes including over 100 new species within six groups (cyrtophorians, hypotrichs s.l., karyorelicteans, oligotrichs, pleurostomatids, and scuticociliates) were isolated and described in detail from observations of live cells and silver-stained specimens. Based on their morphology, morphogene- sis and molecular phylogeny, three new families (Wilbertomorphidae, Kentrophyllidae, Protolitonotidae) and 22 new genera (Apotrachelocerca, Wilbertomorpha, Protolitonotus, Paracyrtophoron, Heterohartmannula, Aporthotrochilia, Falcicyclidium, Paramesanophrys, Pseudodiophrys, Monocoronella, Neourostylopsis, Apobakuella, Parabistichella, Heterokeronopsis, Het- erotachysoma, Antiokeronopsis, Apoholosticha, Pseudogastrostyla, Antestrombidium, Sinistrostrombidium, Williophrya, and Varistrombidium) were established. In the present review, we summarize these studies which show there is a large, undiscovered diversity of ciliates, especially in undersampled habitats, such as subtropical/tropical coastal waters, mangrove wetlands, estuar- ies and aquaculture ponds. We also highlight the importance of integrative approaches, combining morphology, morphogenesis and molecular phylogeny, in order to understand ciliate systematics and ecosystem function. © 2017 Elsevier GmbH. All rights reserved. Keywords: Cyrtophoria; Hypotricha; Karyorelictea; Oligotrichea; Pleurostomatida; Scuticociliatia Introduction ∗ Ciliates have the greatest diversity of cell structure among Corresponding authors. all eukaryotic microorganisms and play significant roles E-mail addresses: [email protected] (H. Ma), [email protected] (H. Pan). in studies of cell biology, genetics, ecology, and evolution 1 All authors contribute equally. http://dx.doi.org/10.1016/j.ejop.2017.04.007 0932-4739/© 2017 Elsevier GmbH. All rights reserved. W. Liu et al. / European Journal of Protistology 61 (2017) 424–438 425 Fig. 1. Sampling sites and habitats. (Hausmann and Bradbury 1996). Over 8000 nominal species ing, scanning electron microscopy, and phylogenetic analyses have been reported to date (Lynn 2008), but most of these mostly of small subunit rRNA (SSU rRNA) gene sequence are known only from living material or from silver-stained data. Morphogenetic processes have also been investigated specimens alone. Consequently, the overwhelming majority for selected taxa. This has resulted in the discovery of nearly of ciliate species are inadequately described by modern stan- 1000 species, mostly from coastal waters of the Bohai Sea, dards (Song et al. 2009; Warren et al. 2017). Furthermore, it Yellow Sea and South China Sea (Song et al. 2009). Since is likely that many species await discovery, especially from 2011, much of this work was supported, or at least facili- undersampled habitats such as the deep ocean and tropical tated, by the International Research Coordination Network marine environments, and it has been estimated that 83–89% for Biodiversity of Ciliates (IRCN-BC) which is funded by of free-living ciliate species are undescribed (Foissner et al. the United States National Science Foundation (NSF) and the 2008). Apart from marine planktonic forms, relatively few Natural Science Foundation of China (NSFC). Here we sum- ciliates have been investigated in terms of their functional marize the findings published during the period 2011–2016 ecology. They tend to be lumped together as a group or guild for six major ciliate groups: cyrtophorians, hypotrichs s.l., in ecological studies rather than having the functional roles karyorelicteans, oligotrichs, pleurostomatids, and scuticocil- of individual species described. Therefore, there is a press- iates. In total, about 210 morphospecies have been isolated ing need for thorough investigations of ciliate biodiversity, and identified of which over 100 are described for the first especially in marine habitats. time. In addition, three new families and 22 new genera have Over the past 25 years a series of investigations have been been established. Although there are other groups which carried out on the ciliate fauna in the temperate and tropical are important and have high diversity, e.g. peritrichs, het- coastal waters of China (Fig. 1). The vast majority of these cil- erotrichs, nassophoreans, they are excluded in the present iates were investigated using a combination of morphological review because relatively few reports focusing on these were and molecular methods, e.g. live observation, silver stain- published during the period 2011–2016. 426 W. Liu et al. / European Journal of Protistology 61 (2017) 424–438 Fig. 2. Selected karyorelicteans from Chinese coastal habitats (original). (A) Apotrachelocerca sp. (B, G) Tracheloraphis spp. (C) Kovalevaia sp. (D, E) Trachelocerca spp. (F) Geleia sp. (H, M) Kentrophoros spp. (I) Wilbertomorpha sp. (J) Apocryptopharynx sp. (K) Loxodes sp. (L) Remanella sp. Scale bars = 200 m (A–D, G); 150 m (E, F, H, M); 20 m (I, J); 40 m (K). Karyorelicteans (Fig. 2A–M) Dragesco 1996). Therefore, knowledge of the infracilia- ture, especially the structure of the oral ciliature, is lacking Karyorelictean ciliates are characterized by their elon- for most species (Dragesco and Dragesco-Kernéis 1986; gated, vermiform, often flattened body shape and numerous Foissner 1995, 1996). non-dividing paradiploid macronuclei that arise from divi- Since 2011, through integrating taxonomic and genetic sion of the micronuclei (Lynn, 2008). It is largely on account methods, we studied 27 marine species of karyorelicteans of this latter character that the class Karyorelictea Corliss, from Chinese coastal waters, including 11 new and nine 1974 is widely considered to represent the ancestral cili- poorly known species, and revised the phylogenetic posi- ate lineage since the non-dividing macronucleus is thought tions of three families based on small subunit (SSU) rRNA to be a primitive character (Corliss 1979). With the excep- gene sequences (Table S1 (in the online version at DOI: tion of the freshwater genus Loxodes Ehrenberg, 1830, all 10.1016/j.ejop.2017.04.007); Xu et al. 2011a,b, 2013, 2015; karyorelicteans are marine and are commonly found in inter- Yan et al. 2015, 2016). The combination of morphological stitial environments (Al-Rasheid 1998). Although it has and molecular data provides strong evidence for our taxo- been nearly two hundred years since the first karyorelictean nomic conclusions. These studies are here summarized. was discovered, few species within this group have been Wilbertomorpha colpoda Xu et al. 2013 was found to rep- studied in detail both in vivo and after protargol staining. resent a new family, Wilbertomorphidae Xu et al., 2013; This is largely because the cells are extremely fragile and because of its unique morphological features. Phylogenetic none have been brought into stable culture (Foissner and analyses based on SSU rRNA gene sequence data support this W. Liu et al. / European Journal of Protistology 61 (2017) 424–438 427 Fig. 3. Selected pleurostomatid ciliates from China seas (original). (A) Protolitonotus sp. (B, E) Litonotus spp. (C, G, H) Amphileptus spp. (D, I, K) Loxophyllum spp. (F, J) Kentrophyllum spp. Scale bars = 150 m (A); 100 m (B, C, E, F); 50 m (D, H, I, J, K). finding with W. colpoda occupying a deep-branching position Pleurostomatids (Fig. 3A–K) between the families Geleiidae Kahl, 1933 and Loxodidae (Xu et al. 2013). Pleurostomatids belong to the class Litostomatea Small Following a detailed reinvestigation of its oral ciliature, and Lynn, 1981. Unlike other litostomateans, members of Trachelocerca arenicola Kahl, 1933 was revealed to rep- the order Pleurostomatida Schewiakoff, 1896 have a lat- resent a new genus, Apotrachelocerca Xu Y. et al., 2011. erally compressed body, conspicuously fewer and shorter After integrating recent morphological and molecular phylo- left somatic kineties, and a ventrally positioned slit-like genetic studies on the family Trachelocercidae Kent, 1881, cytostome (Lynn 2008). two new hypotheses about the evolution of its seven genera Most pleurostomatids are periphytic and can be found