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Mixotrophic Protists Among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology

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Mixotrophic Protists Among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN PhD thesis Woraporn Tarangkoon Mixotrophic Protists among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology Academic advisor: Associate Professor Per Juel Hansen Submitted: 29/04/10 Contents List of publications 3 Preface 4 Summary 6 Sammenfating (Danish summary) 8 สรุป (Thai summary) 10 The sections and objectives of the thesis 12 Introduction 14 1) Mixotrophy among marine planktonic protists 14 1.1) The role of light, food concentration and nutrients for 17 the growth of marine mixotrophic planktonic protists 1.2) Importance of marine mixotrophic protists in the 20 planktonic food web 2) Marine symbiont-bearing dinoflagellates 24 2.1) Occurrence of symbionts in the order Dinophysiales 24 2.2) The spatial distribution of symbiont-bearing dinoflagellates in 27 marine waters 2.3) The role of symbionts and phagotrophy in dinoflagellates with symbionts 28 3) Symbiosis and mixotrophy in the marine ciliate genus Mesodinium 30 3.1) Occurrence of symbiosis in Mesodinium spp. 30 3.2) The distribution of marine Mesodinium spp. 30 3.3) The role of symbionts and phagotrophy in marine Mesodinium rubrum 33 and Mesodinium pulex Conclusion and future perspectives 36 References 38 Paper I Paper II Paper III Appendix-Paper IV Appendix-I Lists of publications The thesis consists of the following papers, referred to in the synthesis by their roman numerals. Co-author statements are attached to the thesis (Appendix-I). Paper I Tarangkoon W, Hansen G Hansen PJ (2010) Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes. Aquat Microb Ecol 58:197-213. Paper II Tarangkoon W, Hansen PJ (Submitted) Prey selection, ingestion and growth responses of the common marine ciliate Mesodinium pulex in the light and in the dark. Aquat Microb Ecol Paper III Hansen PJ, Moldrup M, Tarangkoon W, Garcia-Cuetos L, Moestrup Ø (draft manuscript) Does the marine red tide ciliate Mesodinium rubrum have replaceable symbionts? Appendix-Paper IV Farnelid H, Riemann L, Tarangkoon W, Hansen G, Hansen PJ (Submitted) Putative N2-fixing heterotrophic bacteria associated with dinoflagellate-cyanobacteria consortia in the low-nitrogen Indian Ocean Aquat Microb Ecol Paper I is reprinted with kind permission from Inter-Research 3 Preface This thesis is written as part of the fulfillment of PhD degree from the Faculty of Science, University of Copenhagen. My PhD grant was supported from Rajamangala University Srivijaya, Thailand.During the PhD period, I was based at the Marine Biological Laboratory (MBL), Helsingør. However, Paper I & Appendix-paper IV were based on results from materials sampled during the “Galathea 3” expedition (Leg 7). Heartfelt thanks to my supervisor, Per Juel Hansen, for all his help and kindness throughout my study. I could not have done it without him. Apart from him being a superb supervisor in an academic way (to open my eyes on culture experiments, contribute ecological thinking, guide the writing etc.), he has also solved my many life abroad obstacles during my study (language, finding a place to stay, visa problem, etc). He is always patient, always stimulate me during my difficult moments, and a companion along the way. “Thank you for being you, Per”. I am also grateful for the stimulating contribution of the other co-authors in my 4 papers. It has been a great pleasure to collaborate with you. I am particularly grateful to Torkel G. Nielsen for providing me with the opportunity to join Leg 7 in the “Galathea 3” expedition and sharing environmental data. I also thank other scientists on board, especially Thomas Kiørboe, Andre Visser, Karen Marie Hillingsø, Maria Hastrup Jensen, Carsten Smidt (Captain of HMDS ‘Vædderen’) and his crew for their help during Leg7. Sincere gratitude to Michael Olesen, regardless of what questions I brought up to him e.g. Danes life, religion, relationship, He was always open for an enthusiastic discussion. I am grateful to all members of the plankton group at the MBL, particularly Lasse T. Nielsen, Karen Riisgaard, Louise K. Poulsen, and Morten Moldrup, who always tried to understand my Thai-English accent and were helpful. Special thanks to Morten, who was frequently bothered (questioning, asking for help, etc) by me during all these years. All my officemates, Jane W. Berens, Herik Staahl, Jon Svendsen, Michael van Deurs, Maria F. Steinhausen, Bjørn Tirsgård are thanked for their help and friendly atmosphere. Another special thank is given to Marianne Ernsted, for her help with finding books and big warm hugs when I was frustrated and homesick. Birgit Thorell Lyck, Marriane Saietz, and other staffs at the MBL and the Aquarium also deserve my thanks for their support and help during my study. 4 Many thanks to Marc Staal and Carola Simon for your generous and all thoughtfulness, you guys are my Dutch big brother and sister who have taken good care of me, in my academic as well as during free time through these years. Cátia Carreirra, Christian Lønborg, Alejandro M. Garcia, are thanked for kindly help, making me laugh and having good times even though we have only met at the last phase of my stay in Denmark but your friendship and kindness are memorized. I am also lucky that I met my new Thai friends and their in laws, Worasiri&Urlik Pederson, Akkaraya&Allan Nielsen, Chanchira&Dennis Mølbæk, Atchaneey Chamnansinp. Thanks for your warm hospitality and help. I am deeply grateful to my colleagues at the Marine Science Department, Faculty of Science and Fisheries Technology, Rajamangala University Srivijaya for their support and hard work while I was away. Thanks are specially given to Suwat Tanyaros, for the achieved grant and encouragement, and to Pornthep Wiruchawong for listening to all my problems and being helpful in a general sense. Suree Satapoomin and Ajcharaporn Piumsomboon are appreciated for their help, advice and support. Without their help I might not end up having my PhD in Denmark. I am indebted to Suriyan Saramul for his advice in using Surfer program, Patama Singhruck, Itchika Sivaipram for always being there, listening and understanding all my issues. Last but not least, million thanks are not enough for my beloved family, mom, dad, my sister, my brother, and my grandparents. Without their love, support and beliefs in me, I could never have been strong enough to endure the cold and dark winters in Denmark and finish my PhD. 28th of April 2010 Woraporn (Mam) 5 Summary The mixotrophic protists (= protists which combine heterotrophy and photosynthesis) are common in marine waters around the world. They vary widely in their photosynthetic and ingestion capabilities and they add a further complication to the marine planktonic food web. This thesis focused on 2 groups of mixotrophic protists: 1) symbiont-bearing dinoflagellates and 2) ciliates belonging to the genus Mesodinium spp. The spatial distribution (horizontal and vertical) of symbiont-bearing dinoflagellates (order Dinophysiales, genera Ornithocercus, Histioneis Parahistioneis, Cithoristes, Amphisolenia, Triposolenia) was investigated along a transect from the deep ocean (Indian Ocean) to shallow coastal waters (North West off Australia), as well as on a transect outside Broome (Australia). The symbionts of these dinoflagellates are either prokaryotic (e.g. heterotrophic bacteria, cyanobacteria) or eukaryotic algae. Cell concentrations of these dinoflagellates were very low in these waters (< 4 cells L-1). The ectosymbionts-bearing dinoflagellates were most common and had the highest species diversity in waters characterized by high temperatures (> 28 ºC) and very low nitrogen concentrations (< 0.4µM). Using light and transmission electron microscopy, we could demonstrate that Ornithocercus spp. ingested not only their ectosymbionts but also other prey items (i.e. ciliates). For future research on their physiology, the successful establishment of these organisms in laboratory culture is required. The ciliate genus Mesodinium contains heterotrophic and mixotrophic species (so far only one symbiont containing species M. rubrum has been described). This study investigated the prey selection, photo and feeding physiology of a non-symbiont containing Mesodinium species, M. pulex. The results showed that Mesodinium pulex ingests a variety of prey cells, but that ingestion rates and especially growth rates varied depending upon the diet. The effects of light and prey concentration on photosynthesis, ingestion and growth rate of M. pulex was studied in detail when fed the dinoflagellate Heterocapsa rotundata, The photosynthetic performance of Mesodinium pulex was quite small, amounting for less then 4 % of its carbon uptake, indicating that M. pulex is primarily a heterotrophic species. Despite this, light affected ingestion rates. Ingestion rates increased by a factor of 2 in the light compared to in the dark. Consequently, growth rates also increased in the light. 6 The ciliate Mesodinium rubrum contains symbionts of cryptophyte origin. In the laboratory, our strain of Mesodinium rubrum is normally cultured on cryptophytes within the “Teleaulax clade”. Prey selection of M. rubrum was investigated by offering different prey types (i.e. cryptophytes, dinoflagellate). Mesodinium rubrum ingested all the offered prey, but it could only maintain sustained growth when fed on Teleaulax amphioxeia. To test whether the symbionts of M. rubrum are permanent or temporary (replaceable), M. rubrum cultures were offered preys from 4 different cryptophyte
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