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Functional, Phylogenetic and Host-Geographic Signatures of Labyrinthula Spp. Provide for Putative Species Delimitation and A Functional, Phylogenetic and Host- Geographic Signatures of Labyrinthula spp. Provide for Putative Species Delimitation and a Global-Scale View of Seagrass Wasting Disease Daniel L. Martin, Ylenia Chiari, Emily Boone, Timothy D. Sherman, Cliff Ross, Sandy Wyllie-Echeverria, Joseph K. Gaydos, et al. Estuaries and Coasts Journal of the Coastal and Estuarine Research Federation ISSN 1559-2723 Estuaries and Coasts DOI 10.1007/s12237-016-0087-z 1 23 Your article is published under the Creative Commons Attribution license which allows users to read, copy, distribute and make derivative works, as long as the author of the original work is cited. You may self- archive this article on your own website, an institutional repository or funder’s repository and make it publicly available immediately. 1 23 Estuaries and Coasts DOI 10.1007/s12237-016-0087-z Functional, Phylogenetic and Host-Geographic Signatures of Labyrinthula spp. Provide for Putative Species Delimitation and a Global-Scale View of Seagrass Wasting Disease Daniel L. Martin1,2,3 & Ylenia Chiari1 & Emily Boone4 & Timothy D. Sherman1 & Cliff Ross5 & Sandy Wyllie-Echeverria6,7 & Joseph K. Gaydos2 & Anne A. Boettcher1,8 Received: 29 September 2015 /Revised: 3 March 2016 /Accepted: 6 March 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Seagrass meadows form ecologically and econom- some isolate-host combinations have the potential for host ically valuable coastal habitat on every continental margin cross-infection, and that several modes of transmission can except the Antarctic, but their areal extent is declining by be effective. Taken together, these data provide additional approximately 2–5 % per year. Seagrass wasting disease is a means for delimiting putative species of Labyrinthula,sug- contributing factor in these declines, with the protist gesting at least five seagrass-pathogenic and perhaps ten or Labyrinthula identified as the etiologic agent. To help eluci- more non-pathogenic marine Bspecies^, yielding a working date the role of Labyrinthula spp. in global seagrass declines, definition for ecologists and epidemiologists attempting to we surveyed roughly one fourth of all seagrass species to reconcile the sundry data related to seagrass wasting disease. identify Labyrinthula diversity at the strain and/or species level, combining results from culturing methods and two com- Keywords 18S . SSU . ITS . rDNA . Biogeography . mon nuclear DNA markers: the ITS and 18S regions of the Emerging infectious diseases . Opportunist . Parasite . ribosomal RNA gene complex. After assaying a subset of the Phylogeography . Plant-pathogen interactions . Virulence . resulting isolates (of which 170 were newly sequenced), we Labyrinthulazosterae .Thalassiatestudinum .Zosteramarina produced a cladogenic context for putative seagrass- pathogenic versus non-pathogenic Labyrinthula while also defining host and geographic ranges. Assays also suggest that Introduction pathogenicity is consistently high (when present; and, even when comparing susceptibility of US East- versus West The global ocean as we knew it has undergone considerable Coast Zostera marina hosts) while virulence is variable, that change due to relatively recent human activity, with some of Communicated by Kenneth Dunton Electronic supplementary material The online version of this article (doi:10.1007/s12237-016-0087-z) contains supplementary material, which is available to authorized users. * Daniel L. Martin 4 Department of Biology, University of Richmond, Richmond, VA, [email protected] USA 5 Department of Biology, University of North Florida, Jacksonville, FL, USA 1 Biology Department, University of South Alabama, Mobile, AL, 6 Friday Harbor Laboratories, University of Washington, Friday USA Harbor, WA, USA 2 The SeaDoc Society, Karen C. Drayer Wildlife Health 7 Center of Marine and Environmental Studies, College of Science and Center—Orcas Island Office, University of California at Davis, Math, University of the Virgin Islands, Saint Thomas, VI, USA Eastsound, WA, USA 8 Present address: Embry-Riddle Aeronautical University, 3 Present address: Prescott, AZ, USA Prescott, AZ, USA Estuaries and Coasts the impacts resulting directly or indirectly from disease and Labyrinthula spp. is hindered by a paucity of basic (Jackson 2008, 2010). Over a decade ago ocean ecosystems information on species or strain-level genetic diversity, began receiving more attention related to marine epidemics, biogeographies, host ranges and specificity, and function- with reports indicating that not only is disease a common al roles within this genus. To date, Labyrinthula associ- feature capable of shaping marine communities, but that in- ations have been reported from at least 17 seagrass spe- fectious diseases are on the rise (Harvell et al. 1999, 2002; cies (Armiger 1964; Vergeer and Hartog 1994). Most Lafferty et al. 2004;WardandLafferty2004). For example, often these seagrasses exhibited necrotic lesions that one of the largest marine epidemics is currently underway, were attributed to Labyrinthula infection, but not all iso- with disease decimating populations of some 20 sea star spe- lates produced disease. For example, Muehlstein et al. cies along the northeast Pacific (Hewson et al. 2014). Many (1988) found two morphotypes—one causing disease, factors influencing biogeography and global drivers of emerg- one not—present on Zostera marina (eelgrass). ing or re-emerging infectious diseases in both marine and Similarly, using DNA sequence evidence, Bockelmann terrestrial systems have anthropogenic origins (e.g., climate et al. (2012) identified three phylotypes from Z. marina, change, pollution, acidification, species invasions, of which two were genetically dissimilar to the disease overfishing), with climate warming a chief concern among producing isolate. Neither of these studies nor the study them (Daszak et al. 2000; Dobson and Foufopoulos 2001; that provided the original 18S rDNA identification of L. Lafferty et al. 2004; Lafferty 2009; Doney et al. 2012; Burge zosterae (Leander and Porter 2001) paired sequencing et al. 2014; but also see Wilson 2009; Epstein 2010). directly with pathogenicity testing for their isolates. Although the drivers have not always been clear for seagrass However, Brakel et al. (2014) did pair geographically wasting disease epidemics, seagrasses are long known for based isolate assays and sequencing, but specifically for their associations with an osmotrophic protist capable of pro- L. zosterae and only within European eelgrass beds. ducing this disease: Labyrinthula zosterae (or related Thus, at the time of this analysis, the only studies to Labyrinthula spp.) has been implicated in seagrass die-offs couple broader assays (across-host-species and large geo- since the 1930s, including one large-scale event (temperate graphic ranges) of isolate pathogenicity with molecular north Atlantic basin) and numerous smaller-scale events in identification are from terrestrial systems, which suggest both the northern and southern hemispheres (reviewed in a hidden diversity of pathogenic and non-pathogenic Sullivan et al. 2013). Labyrinthula for Poaceae hosts (Craven et al. 2005; Labyrinthula spp. belong to the monotypic family Douhan et al. 2009). Nevertheless, while the higher clas- Labyrinthulidae (Anderson and Cavalier-Smith 2012), sification of Labyrinthulidae has seen progress (Adl et al. which to date includes mostly marine forms that glide 2005, 2007;Tsuietal.2009; Anderson and Cavalier- within a communal network of ectoplasm. This shared Smith 2012;Beakesetal.2014), the elucidation of network earned them a reference as net slime molds, but Labyrinthula species has been paltry. Regardless of dis- they have no close relation to the more traditional slime tinction, outbreaks of seagrass wasting disease have had molds (now of the Amoebozoa; Adl et al. 2005), nor to significant impacts on coastal ecosystems. the Fungi. Some eleven species of Labyrinthula are cur- Seagrass meadows themselves form ecologically and eco- rently recognized, but are difficult to distinguish from one nomically valuable coastal habitat on every continental mar- another on the basis of morphology alone (Dick 2001; gin except the Antarctic (Short and Wyllie-Echeverria 1996; Bigelow et al. 2005). Significantly, only two epithets, Kenworthy et al. 2006;Orthetal.2006;Duarteetal.2008; zosterae (Muehlstein et al. 1991)andterrestris (Bigelow Waycott et al. 2009;Duarteetal.2013). To help elucidate the et al. 2005), have been applied to sequences from genetic diversity, host specificity, geographic range, and path- Labyrinthula isolates available in public databases. In ogenicity of Labyrinthula spp. associated with seagrasses contrast, culture-independent studies of environmental from around the world, we surveyed roughly one quarter of 18S rDNA sequences imply that several, and likely many, all seagrass species to identify Labyrinthula at the strain and/ species of Labyrinthula are typically present in marine or species level using a combination of parasite culturing and ecosystems (e.g., Collado-Mercado et al. 2010). phylogenetic analyses. We used two common nuclear DNA Functional roles for most types are incompletely known, markers, the ITS1-5.8S-ITS2 (ITS) and the small subunit but range from strict saprobes and endophytic parasites (SSU, or 18S) regions of the ribosomal RNA gene complex. (Raghukumar and Damare 2011), to the lesser-known as A subset of these isolates was assayed for their
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