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A practical guide to new nomenclature for species within the “Alexandrium tamarense species complex”

Article · October 2018

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The user has requested enhancement of the downloaded file. A practical guide to new nomenclature designation of the Group I ribotype as A. fundyense. for species within the “Alexandrium The controversy regarding the tamarense species complex” Group I designation centers on whether the cells used for the original A. catenel- la description were from Group I or IV, For several decades, the “Alexandrium ITS2 complementary base pair changes, given that populations of both species tamarense species complex” included saxitoxin production and the presence in the Pacific are known to exhibit the three morphologically defined spe- or absence of a key gene involved in classic “A. catenella” morphotype. Mo- cies, A. catenella, A. fundyense, and A. saxitoxin synthesis. These combined lecular analyses of “A. catenella” cells tamarense [1]. Worldwide, the group data fully support the conclusion that collected from the coast of California at is one of several responsible for para- the Group I–V ribotypes are distinct Redondo Beach [13] and Monterey Bay lytic shellfish poisoning, a potentially species. [14], south of the type location, indi- life-threatening syndrome that occurs Equally important, the morphologi- cated that these cells belonged to Group following the consumption of shellfish cal analysis by John et al. [8] showed I (Fig. 1). Further, there is no evidence contaminated with paralytic shellfish no single morphological trait, or that any species except Group I occurs toxins (saxitoxin and analogs). Mor- suite of traits, corroborated the in all of the Americas [5, 13-17]. Use phologically, Alexandrium catenella was original morphospecies descrip- of species-specific molecular assays in distinguished by rounded, slightly ante- tions, nor could any combination of other parts of the world, however, have rior-posteriorly compressed cells, chain morphological traits distinguish the shown Group I and IV cells matching formation, and a 1’ plate lacking a ven- ribotype groups from one another. the A. catenella morphotype co-occur tral pore [1, 2]. Alexandrium fundyense There was simply too much overlap in (see Fig. 1 and associated references). and A. tamarense shared the same Ko- the morphologies expressed by each of The lack of any extant type material for foidian plate tabulation as A. catenella, the ribotype groups for morphological molecular testing and the overlapping but typically exhibited less compressed characters to prove useful. For example, distributions of Group I and IV cells cellular morphologies [1, 3]. Alexan- Group I populations in the entire north exhibiting the “A. catenella” morphol- drium tamarense and A. fundyense were Atlantic and north Pacific including ogy in other regions creates uncertain- distinguished based on the presence of Alaska exhibit both “A. fundyense” and ty about which ribotype was described a ventral pore on the 1ʹ plate in A. tama- “A. tamarense” morphology. In contrast, originally. Based partially on this uncer- rense and its absence in A. fundyense [1]. those in the eastern Pacific from San tainty, John et al. [4] submitted a formal Field and culture studies over the Francisco Bay south to Chile, the south- proposal to Taxon for rejection of the past 20 years often described “A. tama- east Atlantic coast of South Africa and name Alexandrium catenella in favor of rense species complex” cells exhibit- many areas in the western Pacific from A. fundyense. ing intermediate morphologies when Australia to Japan, frequently form mul- A second reason for using the A. compared to the original descriptions ti-cell chains, a signature of the original fundyense name in lieu of A. catenella is of all three species (see John et al. [4] “A. catenella” morphological descrip- that a large volume of literature regard- for a summary). Phylogenetic studies tion. These latter Group I populations ing Group I blooms, especially from the of rDNA gene sequences obtained from also display the typical “A. catenella” Gulf of Maine, has been published using “A. tamarense complex” isolates fall into morphology and are indistinguishable the name A. fundyense. Continued use one of five distinct ribotype groups. from the Group IV populations found in of A. fundyense would cause less dis- These do not correlate with the original the Western Pacific (South Japan, Korea ruption to the existing documentation morphologically defined species and and China) and the Mediterranean Sea and serve the International Code of No- were initially designated as Groups I–V [5, 9, 10, 12]. menclature (ICN) Article 14.2 goal that [5-8]. The genetic distances among the Based on their analyses, John et al. states: “Conservation aims at retention ribotypes are typical of those separat- [8] assigned the following species des- of those names that best serve stability ing other dinoflagellate species. Togeth- ignations to each ribotype group: A. of nomenclature”. A third reason for re- er, these observations indicate that the fundyense (Group I), A. mediterraneum jecting A. catenella, and assigning Group original species descriptions depicted a (Group II), A. tamarense (Group III), A. I to A. fundyense and Group IV to A. pa- series of “morphotypes” shared by vari- pacificum (Group IV) and A. australiense cificum, was to provide the scientific ous species in the A. tamarense complex (Group V). John et al. [8] took further community a means of unambiguously rather than actual species. Consequent- steps to provide exhaustive morpho- distinguishing the Group I and IV cells ly, researchers set out to confirm that logical and genetic descriptions and exhibiting the same A. catenella mor- the five ribotypes represented separate submitted holotype and epitype mate- photype, especially in regions where species (e.g., [5, 8-11]). The most com- rial, as appropriate, to the Herbarium they are sympatric. prehensive of these efforts by John et al. Senckenbergianum (FR) in the Centre Based on the known distribution of [8] assembled diverse lines of evidence, of Excellence for Dinophyte Taxonomy Group I cells along the coast of North including detailed morphological analy- (Wilhelmshaven, Germany). Most of and South America, Fraga et al. [18] ses, rDNA phylogenies, mating incom- these nomenclatural reassignments submitted a counterproposal to Taxon patibility assessments, ITS1/5.8S/ITS2 raised minimal concerns among taxon- against rejecting the name A. catenella. rDNA uncorrected genetic distances, omists. The primary exception was the The authors argued that the Group I

HARMFUL ALGAE NEWS NO. 61 / 2018 13 Fig. 1. Known locations where Group I A. catenella (red dots) and Group IV A. pacificum (yellow dots) cells have been collected and confirmed with molecular assays [6-8, 11, 12, 15-17, 20-37]. The yellow line and yellow arrow on the west coast of North America indicates the type locality for A. catenella. The white arrow shows the type locality for A. fundyense in the Bay of Fundy, Canada. The single report of A. catenella in the Mediterranean and A. pacificum in the Drake Passage between South America and Antarctica should be considered provisional until additional isolates were identified in both regions. No isolates of Alexandirum catenella have been obtained for the Mediterranean Sea despite extensive sampling and though Busch et al. [34] detected putative A. catenella sequences from environmental DNA samples collected from Fangar Bay (Catalan coast) using 454 pyrosequencing of LSU rDNA, the reads are so short they cannot be considered as definitive. If A. catenella does occur in the Mediterranean it may represent a recent introduction. distribution in the type locale was suf- to be aware of this nomenclatural 1. You work in a region where co-oc- ficiently established to conclude only change as it will affect reporting curring members of the “Alexandri- Group I cells were used for the original requirements, communication with um tamarense species complex” are A. catenella description (Fig. 1). If true, the public, and use of past literature present. Based on their morphology, the ICN rules of priority, in cases where when developing strategies for deal- you have assigned them the names the type material is not in question, ing with paralytic shellfish poison- A. catenella and A. tamarense. What clearly dictates retention of the name ing events and regulations. do you do? “A. catenella” for Group I because it was 3. This decision also places significant • You need to sequence barcoding published prior to the “A. fundyense” demands on future researchers as marker regions from the strains, Group I description [1, 2]. they investigate the literature. For specifically, ribosomal RNA genes Nomenclature change proposals example, with the exception of Chil- or use species-specific molecular such as those of John et al. [4] and Fraga ean and South African research, assays. Only then can you truly et al. [18] are adjudicated by The ICN most of the papers published on “A. determine the species present, Nomenclature Committee for Algae. catenella” before 2015 represent i.e. A. australiense, A. catenella, A. This committee met to consider the reports of the morphologically in- mediterraneum, A. pacificum, or proposals and ruled the name Gonyaul- distinguishable species A. pacificum. A. tamarense. ax catenella (Alexandrium catenella) Similarly, future workers will need • A particular case is that from should not be rejected and that A. fundy- to recognize the extensive literature Japan, where species typically ense and A. catenella are conspecific with published between 1985 and 2017 identified as A. catenella should nomenclatural priority being given to A. regarding Group I A. fundyense actu- be called A. pacificum, and the catenella [19]. For the valid names and ally refers to A. catenella. species recognized as A. tama- synonymy one can refer to the follow- 4. The formal assignment of the name rense should be designated as A. ing checklist: https://www.dinophyta. A. catenella to Group I also means catenella. org/checklists/of-species/alexandrium/­ . this name cannot apply to Group 2. You are working on an isolate from IV (A. pacificum) despite Group IV a culture collection identified as Al- The decision of the Nomenclature Com- exhibiting morphologies exactly exandrium catenella. Cells have the mittee has the following implications: matching the original A. catenella typical morphology of A. catenella 1. All publications involving Group I description. as described by Whedon and Kofoid cells published using the name A. 5. Ribotype groups II, III and V species [2]. When you sequence its riboso- fundyense should now be considered should be referred to as A. mediter- mal RNA genes, you discover that it A. catenella. raneum, A. tamarense and A. aus- is the A. pacificum (Group IV) geno- 2. This nomenclatural revision affects traliense, respectively [8]. type. What do you do? the two most widespread toxic spe- • The isolate should be reclassified cies (Group I and IV) within the “A. Example scenarios clarifying how to as A. pacificum. tamarense complex”. Resource man- identify and name “Alexandrium tama- 3. The typical toxic bloom-forming or- agers in much of the world need rense complex” species: ganism that occurs in your region

14 HARMFUL ALGAE NEWS NO. 61 / 2018 is well known and has always been pose. It is further recommended that 24. Genovesi B et al. 2011. J Plank Res 33: known as Alexandrium fundyense or the harmful algae research community 405-414 A. tamarense. It has the Group I gen- work to identify and standardize a set 25. Anderson DM et al. 2012. Harmful Algae 14: 10-35 otype. What do you do? of molecular assays to be used when 26. Baggesen C et al 2012. Harmful Algae 19: • You refer to the species as A. screening samples for these species. All 108-116 catenella. publications regarding these species 27. Murray SA et al 2012 Harmful Algae 18: 4. Toxic and non-toxic strains with the should include both the Group I–V ri- 96-104 morphology of Alexandrium tama- botype designations and species names. 28. Gu HF et al 2013. Harmful Algae 27: 68- 81 rense coexist in your region. What This will ensure unambiguous species 29. Bolch C et al 2014. In: 16th ICHA, Welling- do you do? identifications and reduce further con- ton, New Zealand 27-31 October 2014. • Molecular barcoding or sequenc- fusion in the literature. The routine Book of Abstracts p 29 ing is mandatory. use of multiple, standardized, species- 30. Fertouna-Bellakhal M et al 2014. Mar • In the case of Scotland, the non- specific molecular assays will also al- Pollut Bull 84: 347-362 31. Zou C et al 2014. Mar Pollut Bull 89: 209- toxic strains correspond to A. low better definition of species ranges, 219. tamarense, while the toxic ones avoid any biases regarding which spe- 32. Dias PJ et al 2015. Bioinvasions Rec 4: are A. catenella. cies are present in a region and identify 233-241 • In the case of the Mediterrane- when new introductions have occurred. 33. Genovesi B et al 2015. Mar Pollut Bull 98: 95-105 an Sea, the non-toxic species A. 34. Busch JA et al. 2016. Harmful Algae 55: tamarense and A. mediterraneum References 191-201 may coexist. The toxic A. pacifi- 1. Balech E 1995. Sherkin Island Marine 35. Shin HH et al 2017. Harmful Algae 68: cum also occurs in this region but Station Publication, Sherkin Island, Co., 31-39 Cork, Ireland typically forms chains. 36. Subong BJ et al 2017. Philipp J Sci 2. Whedon WF & CA Kofoid 1936. Univer- 146:421-423 5. Chain forming cells of the “Alexan- sity of California Publications in Zoology 37. Fabro E et al 2017. J Phycol 53: 1206- drium tamarense complex” are ob- 41: 25-34 1222 served. What do you do? 3. Balech E 1985. In: Toxic Dinoflagellates • Start with the hypothesis that if (Elsevier, New York), pp 33–38 4. John U et al 2014. Taxon 63: 932-933 it is a high latitude, cold-water Authors 5. Lilly EL et al 2007. J Phycol 43: 1329- R. Wayne Litaker, NOAA, Beaufort, North area, the species present is A. 1338 Carolina, United States catenella, but if it is a warm tem- 6. Penna A et al 2008. Eur J Phycol 43: 163- perate area, it is A. pacificum, 178 Santiago Fraga, IEO, Centro Oceanográfico 7. Miranda LN et al 2012. Harmful Algae then confirm using molecular as- de Vigo, Vigo, Spain (*now retired) 16: 35-48 says. 8. John U et al 2014. Protist 65: 779-804 Marina Montresor, Stazione Zoologica Anton 6. Special attention should be given to 9. Scholin CA et al 1994. J Phycol 30: 999- Dohrn, Napoli, Italy the non-toxic A. affine. Initially, this 1011 species was not considered part of 10. John U et al 2003. Mol Biol Evol 20: Michael Brosnahan & Donald M Anderson, 1015-1027 the “Alexandrium tamarense spe- WHOI, Woods Hole, Massachusetts, USA 11. Wang L et al 2014. Harmful Algae 31: cies complex” because it could be 100-113 Mona Hoppenrath, Senckenberg am Meer, morphologically identified by the 12. Gao Y et al 2015. Mar Pollut Bull 96: 210- German Center for Marine Biodiversity position of the anterior attachment 219 Research, Wilhelmshaven, Germany pore. However, the anterior attach- 13. Garneau ME et al 2011. Appl Environ Microbiol 77: 7669-7680 ment pore can be absent in old cells, Shauna Murray, University of Technology 14. Jester R et al. 2009. Harmful Algae 8: Sydney, Australia making it an unreliable morphologi- 291-298 cal character leaving A. affine mor- 15. Jedlicki A et al 2012. AoB Plants. 12. doi: Jennifer Wolny, Maryland Department of phologically indistinguishable from 10.1093/aobpla/pls033 Natural Resources, Annapolis, Maryland, USA the “Alexandrium tamarense species 16. Varela D et al 2011. Harmful Algae 15: 8-18 complex”. Uwe John, Alfred-Wegener-Institute Helm- 17. Vandersea et al 2017. Phycologia 56(3): holtz Center for Polar and Marine Research, 303-320 Bremerhaven, Germany; Helmholtz Institute Alexandrium tama- In conclusion, the “ 18. Fraga S et al 2015. Taxon 64: 634-635 for Functional Marine Biodiversity, Olden- rense complex” currently includes 19. Prud’homme van Reine WF 2017. Taxon burg, Germany. the following five species: A. catenella 6: 197-198 20. Bolch CJS & MF de Salas 2007. Harmful (Group I), A. mediterraneum (Group II), Nagore Sampedro, Institut de Ciències del Algae 6: 465-485 Mar-CSIC, Barcelona, Spain A. tamarense (Group III), A. pacificum 21. Penna A & L Galluzzi 2008. In: Algal A. australiense (Group IV) and (Group Toxins: Nature, Occurrence, Effect and Jacob Larsen, IOC Science and Communica- V). Multiple analyses clearly show these Detection (NATO Science for Peace and tion Centre on Harmful Algae, University of species cannot be distinguished based Security Series A-Chemistry and Biology Copenhagen, Denmark (Springer Netherlands),pp. 261-283 on morphology. Instead, species-spe- 22. Masseret E et al 2009. Appl Environ cific molecular assays are required for António J. Calado, Biology and GeoBioTec Microbiol 75: 2037-2045 Research Unit, University of Aveiro, Portugal reliable identification. Vandersea et al. 23. Chambouvet A et al 2011. Res Microbiol [17] provided an overview of the vari- 62: 959-968 Email: [email protected] ous assays that can be used for this pur-

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