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Intracellular Eukaryotic Pathogens in Brown Macroalgae in the Eastern Mediterranean, Including LSU Rrna Data for the Oomycete Eurychasma Dicksonii

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Intracellular Eukaryotic Pathogens in Brown Macroalgae in the Eastern Mediterranean, Including LSU Rrna Data for the Oomycete Eurychasma Dicksonii Vol. 104: 1–11, 2013 DISEASES OF AQUATIC ORGANISMS Published April 29 doi: 10.3354/dao02583 Dis Aquat Org Intracellular eukaryotic pathogens in brown macroalgae in the Eastern Mediterranean, including LSU rRNA data for the oomycete Eurychasma dicksonii Martina Strittmatter1,2,6, Claire M. M. Gachon1, Dieter G. Müller3, Julia Kleinteich3, Svenja Heesch1,7, Amerssa Tsirigoti4, Christos Katsaros4, Maria Kostopoulou2, Frithjof C. Küpper1,5,* 1Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK 2University of the Aegean, Department of Marine Sciences, University Hill, 81 100 Mytilene, Greece 3Universität Konstanz, FB Biologie, 78457 Konstanz, Germany 4University of Athens, Faculty of Biology, Athens 157 84, Greece 5Oceanlab, University of Aberdeen, Main Street, Newburgh AB41 6AA, UK 6Present address: CNRS and UPMC University Paris 06, The Marine Plants and Biomolecules Laboratory, UMR 7139, Station Biologique de Roscoff, Place Georges Teissier, CS 90074, 29688 Roscoff Cedex, France 7Present address: Irish Seaweed Research Group, Ryan Institute, National University of Ireland Galway, University Road, Galway, Ireland ABSTRACT: For the Mediterranean Sea, and indeed most of the world’s oceans, the biodiversity and biogeography of eukaryotic pathogens infecting marine macroalgae remains poorly known, yet their ecological impact is probably significant. Based on 2 sampling campaigns on the Greek island of Lesvos in 2009 and 1 in northern Greece in 2012, this study provides first records of 3 intracellular eukaryotic pathogens infecting filamentous brown algae at these locations: Eury - chas ma dicksonii, Anisolpidium sphacellarum, and A. ectocarpii. Field and microscopic observa- tions of the 3 pathogens are complemented by the first E. dicksonii large subunit ribosomal RNA (LSU rRNA) gene sequence analyses of isolates from Lesvos and other parts of the world. The lat- ter highlights the monophyly of E. dicksonii worldwide and confirms the basal position of this pathogen within the oomycete lineage (Peronosporomycotina). The results of this study strongly support the notion that the geographic distribution of the relatively few eukaryotic seaweed pathogens is probably much larger than previously thought and that many of the world’s marine bioregions remain seriously undersampled and understudied in this respect. KEY WORDS: Brown algae · Pathogens · Oomycetes · Hyphochytrids · Infection · Eastern Mediterranean Sea · Phylogeny · LSU rRNA · SSU rRNA · cox2 Resale or republication not permitted without written consent of the publisher INTRODUCTION (reviewed by Gachon et al. 2010). Much of the cur- rent knowledge of macroalgal-associated pathogens Like any other group of living organisms, seaweeds is based on decade- or century-old reports derived are subject to a permanent onslaught of a range of from field studies and is therefore limited to light pathogens including viruses, bacteria, fungi, oomy - microscopic observations and morphological classifi- cetes, plasmodiophoraleans and endophytic algae cation. Although dating back half a century, Spar- *Corresponding author. Email: [email protected] © Inter-Research 2013 · www.int-res.com 2 Dis Aquat Org 104: 1–11, 2013 row’s (1960) monograph remains unsurpassed for the port in particular enhances the spread of microorgan- identification of marine fungi and fungus-like organ- isms, including pathogens, while anthropogenic pollu- isms. His terminology of aquatic phycomycetes, no tion may favour disease outbreaks (Ruiz et al. 2000). longer in use, includes a polyphyletic group of zoo- As in the terrestrial environment, the successful es- sporic fungi and fungus-like organisms, mostly chytri - tablishment and propagation of introduced species diomycetes, oomycetes and hyphochytridiomycetes, might at least to some extent be due to missing patho- with the latter 2 actually being heterokonts (stra- gens controlling alien seaweed populations in contrast menopiles). In most cases, such pathogens are holo- to established pathogens controlling native popula- carpic, biotrophic and intracellular. In many cases, a tions (Torchin et al. 2003). Conversely, the introduction pathogen infection observed by light microscopy of a generalist pathogen is known to have devastating may have symptoms resembling non-pathological, effects on native species (Andreou et al. 2012). Re- subcellular structures of host cells, which are hard to cently, the importance of pathogen spread and syner- distinguish by untrained observers. These features gistic effects with abiotic stressors has come to light make their observation in field-collected material, on the sea grass wasting disease caused by the protist but also their study in culture, particularly difficult. Laby rin thula sp. affecting sea grass populations in the The ecological role of zoosporic fungi and fungus- Mediterranean Sea and worldwide (McKone & Tanner like organisms is increasingly recognized in aquatic 2009, Garcias-Bonet et al. 2011). Importantly, it pro- ecosystems, and those organisms represent an im- vides one of the scarce examples on the impact of in- portant and non-negligible part of the microbial loop fectious diseases on aquatic plants and, although not (Gleason et al. 2011, Sime-Ngando et al. 2011). Fur- well studied, similar scenarios can be assumed for thermore, previously unknown taxa are described at seaweeds. Therefore, macroalgal pathologies cannot high rates in freshwater and marine systems, includ- be neglected either from an ecological point of view ing parasites of algae. Nevertheless, the knowledge or from an applied perspective considering macro- of fungal-like organisms parasitizing macroalgae is algae as sources of nutrients and biofuels. However, by far less substantial compared to phytoplankton. correct assessment of changes in pathogen popula- This situation has certainly been driven by the strong tions can only be made if baseline data are available research interest in the dynamics of diatom, cocco- allowing determination of the frequency of infection lithophore and dinoflagellate blooms (Park et al. and pathogen species compositions linked to abiotic 2004, Chambouvet et al. 2008, Ibelings et al. 2011). factors and pollution. Overall, the biodiversity and biogeography of algal The objective of the present study was to investi- pathogens remains very poorly known in most of the gate the occurrence of eukaryotic pathogens affect- world’s seas. Traditionally, study areas were often in ing brown seaweeds in the Eastern Mediterranean proximity to the investigators’ home countries, result- Sea. Observation of filamentous brown algal hosts by ing in parts of the world that are comparatively well microscopy resulted in the detection of Eury chasma covered such as the European North Atlantic and dicksonii (E. P. Wright) Magnus and 2 intracellular both coasts of North America (Marano et al. 2012), pathogens identified as members of the genus Ani - whereas vast regions remain under- or unstudied, in solpidium. Furthermore, we report here the first gene particular warmer seas. While substantial, but proba- sequences of large subunit ribosomal RNA (LSU bly incomplete, records on the macroalgal flora are rRNA) for E. dicksonii, which has re cently been used available from the Eastern Mediterranean Sea (Par - to delineate early-branching oomycete clades (Mu - lakay et al. 2005, Tsiamis et al. 2010, 2013a), macro - raosa et al. 2009, Macey et al. 2011). The LSU rRNA algal diseases in this region historically have not gene sequence information from E. dicksonii isolates been investigated. originating from the Pacific, South and Northeast The Mediterranean Sea is a prominent example of Atlantic Ocean and the Aegean Sea not only con- an ecosystem with a multitude of human impacts. De- firms the identification of the Greek pathogen with spite a trend towards re-oligotrophication of coastal molecular tools, but also underscores the monophyly areas due, in particular, to more widespread sewage of Eurychasma on a global scale. Finally, a phyloge- treatment (Tsiamis et al. 2013b), it remains a hotspot netic analysis of combined LSU rRNA, small subunit for alien species introductions, a number of those (SSU) rRNA and mitochondrial cytochrome c oxidase being invasive. Many of them are thought to have subunit 2 (cox2) data confirms the basal position of entered the Mediterranean via the Suez Canal (so- Eurychasma among the oomycetes. The marker cox2 called Lessepsian migration; Boudouresque & Ver- was in cluded since it is an established locus for phy- laque 2002, Streftaris & Zenetos 2006). Marine trans- logenies of marine oomycetes (Cook et al. 2001). Strittmatter et al.: Eukaryotic pathogens in Mediterranean macroalgae 3 MATERIALS AND METHODS immediately transferred into seawater and stored at ambient temperature until further analysis. Macro- Sampling and microscopic observation scopically, disease was never discernible, and sam- ples were thus collected from the field in an unbiased Algal material was collected in the Aegean Sea manner. (Greece), around the coastline of Lesvos (39° 10’ N, In the laboratory, specimens were examined for the 26° 20’ E) in February and March 2009 and around presence of intracellular pathogens using conven- the small island of Panagia/Astris (40° 33’ N, 24° 37’ E) tional bright field microscopy (Olympus CH 20). Par- off the south coast of Thasos Island in early May ticular focus was on the detection of characteristic 2012. Particular focus was on filamentous brown pathogen
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