Advertisement

Marine Biodiversity

, Volume 49, Issue 2, pp 749–758 | Cite as

Towards global distribution maps of unicellular organisms such as calcareous dinophytes based on DNA sequence information

  • Anže Žerdoner Čalasan
  • Juliane Kretschmann
  • Natalia H. Filipowicz
  • Ramona-Elena Irimia
  • Monika Kirsch
  • Marc GottschlingEmail author
Original Paper
  • 143 Downloads

Abstract

Despite recent fruitful attempts to elucidate microbial biogeography in more detail, knowledge of distribution still lags behind for dinophytes. Evolutionary phenomena, such as cryptic speciation and modification due to the environment, hamper reliable conclusions about the distribution of this important plankton group. We combined newly collected samples from the Black Sea (ten new strains from three localities) with occurrence data, which have been gathered extensively over the past decade, in order to provide the first global distribution maps of four specific ribotypes assigned to the Scrippsiella lineage (Thoracosphaeraceae, Peridiniales) collected at a total of 39 sites. They showed a wide, partly overlapping distribution and shared the presence primarily at the coastal localities. Differences in abundance of specific ribotypes were observed, but the ribotype corresponding to the globally most frequently encountered species Scrippsiella acuminata has not yet been found in the Black Sea. We discuss the significance of DNA-based records for distribution maps particularly of unicellular organisms such as dinophytes. Based on a collective approach as exemplified in our study, we may start to understand in detail the ecological basis and the dynamics of the individual colonisation/invasion events, species establishment and consequent distribution in the microbiome, all of which have been changing drastically due to the ongoing climate change.

Keywords

Biogeography Black Sea Dinoflagellates Dispersal Niche 

Notes

Acknowledgments

We are thankful to all colleagues who have contributed to the global collection of dinophytes over the past years. We thank Nina Simanovic for improving the English version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Sampling and field studies

The study was performed in compliance with the Convention on Biological Diversity (CBD).

Supplementary material

12526_2018_848_MOESM1_ESM.pdf (107 kb)
ESM 1 (PDF 106 kb)

References

  1. Aguilar M, Lado C (2012) Ecological niche models reveal the importance of climate variability for the biogeography of protosteloid amoebae. ISME J 6:1506–1514CrossRefGoogle Scholar
  2. Aguilar M, Fiore-Donno AM, Lado C, Cavalier-Smith T (2014) Using environmental niche models to test the 'everything is everywhere' hypothesis for Badhamia. ISME J 8:737–745CrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  4. Bakan G, Büyükgüngör H (2000) The Black Sea. Mar Pollut Bull 41:24–43CrossRefGoogle Scholar
  5. Boenigk J, Ereshefsky M, Hoef-Emden K, Mallet J, Bass D (2012) Concepts in protistology: species definitions and boundaries. Eur J Protistol 48:96–102CrossRefGoogle Scholar
  6. Caron DA (2009) Past president's address: Protistan biogeography: why all the fuss? J Eukaryot Microbiol 56:105–112CrossRefGoogle Scholar
  7. Cuvelier ML, Allen AE, Monier A, McCrow JP, Messie M, Tringe SG, Woyke T, Welsh RM, Ishoey T, Lee JH, Binder BJ, DuPont CL, Latasa M, Guigand C, Buck KR, Hilton J, Thiagarajan M, Caler E, Read B, Lasken RS, Chavez FP, Worden AZ (2010) Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natl Acad Sci U S A 107:14679–14684CrossRefGoogle Scholar
  8. Dolan JR (2011) The legacy of the last cruise of the Carnegie: a lesson in the value of dusty old taxonomic monographs. J Plankton Res 33:1317–1324CrossRefGoogle Scholar
  9. Elbrächter M, Gottschling M, Hildebrand-Habel T, Keupp H, Kohring R et al. (2008) Establishing an agenda for calcareous dinoflagellates research (Thoracosphaeraceae, Dinophyceae) including a nomenclatural synopsis of generic names. Taxon 57:1289–1303CrossRefGoogle Scholar
  10. Elferink S, Gottschling M, John U, Töbe K, Voß D, Neuhaus S, Zielinski O, Lundholm N, Koch B, Krock B, Cembella A, Wohlrab S (2017) Molecular diversity patterns among various phytoplankton size-fractions in West Greenland in late summer. Deep-Sea Res I 121:54–69CrossRefGoogle Scholar
  11. Evans KM, Chepurnov VA, Sluiman HJ, Thomas SJ, Spears BM, Mann DG (2009) Highly differentiated populations of the freshwater diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist 160:386–396CrossRefGoogle Scholar
  12. Fenchel T (2005) Cosmopolitan microbes and their ‘cryptic’ species. Aquat Microb Ecol 41:49–54CrossRefGoogle Scholar
  13. Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL (1993) A classification of living and fossil dinoflagellates. Micropaleontol Spec Publ:1–245Google Scholar
  14. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Environ Microbiol 296:1061–1063Google Scholar
  15. Foissner W (2007) Dispersal and biogeography of protists: recent advances. Jpn J Protozool 40:1–16Google Scholar
  16. Fritz SA, Schnitzler J, Eronen JT, Hof C, Böhning-Gaese K, Graham CH (2013) Diversity in time and space: wanted dead and alive. Trends Ecol Evol 28:509–516CrossRefGoogle Scholar
  17. Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK (2012) Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol 27:47–56CrossRefGoogle Scholar
  18. Gobler CJ, Doherty OM, Hattenrath-Lehmann TK, Griffith AW, Kang Y, Litaker RW (2017) Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North Atlantic and North Pacific oceans. Proc Natl Acad Sci U S A 144:4975–4980CrossRefGoogle Scholar
  19. Gómez F, Boicenco L (2004) An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia 517:43–59CrossRefGoogle Scholar
  20. Gottschling M (2008) Aktuelle Herausforderungen für Diversitätserfassung und Systematik: Blütenpflanzen, Kalkige Dinoflagellaten und Papillomviren im Vergleich. FU Berlin, Berlin (Habilitation thesis; www.sysbot.biologie.uni-muenchen.de/en/people/gottschling/gottschling_habil.pdf ), 33p
  21. Gottschling M, Kirsch M (2009) Annotated list of Scandinavian calcareous dinoflagellates collected in fall 2003. Berl Paläobiol Abh 10:193–198Google Scholar
  22. Gottschling M, Knop R, Plötner J, Kirsch M, Willems H, Keupp H (2005) A molecular phylogeny of Scrippsiella sensu lato (Calciodinellaceae, Dinophyta) with interpretations on morphology and distribution. Eur J Phycol 40:207–220CrossRefGoogle Scholar
  23. Gottschling M, Söhner S, Zinßmeister C, John U, Plötner J, Schweikert M, Aligizaki K, Elbrächter M (2012) Delimitation of the Thoracosphaeraceae (Dinophyceae), including the calcareous dinoflagellates, based on large amounts of ribosomal RNA sequence data. Protist 163:15–24CrossRefGoogle Scholar
  24. Gu H, Kirsch M, Zinßmeister C, Söhner S, Meier KJS, Liu T, Gottschling M (2013) Waking the dead: morphological and molecular characterization of extant †Posoniella tricarinelloides (Thoracosphaeraceae, Dinophyceae). Protist 164:583–597CrossRefGoogle Scholar
  25. Hall TA (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61Google Scholar
  26. Hallegraeff GM, Bolch CJ (1992) Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. J Plankton Res 14:1067–1084CrossRefGoogle Scholar
  27. Heibl C, Renner SS (2012) Distribution models and a dated phylogeny for Chilean Oxalis species reveal occupation of new habitats by different lineages, not rapid adaptive radiation. Syst Biol 61:823–834CrossRefGoogle Scholar
  28. Janofske D (2000) Scrippsiella trochoidea and Scrippsiella regalis, nov. comb. (Peridiniales, Dinophyceae): a comparison. J Phycol 36:178–189CrossRefGoogle Scholar
  29. John U, Litaker RW, Montresor M, Murray S, Brosnahan ML, Anderson DM (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779–804CrossRefGoogle Scholar
  30. Kohli GS, Neilan BA, Brown MV, Hoppenrath M, Murray SA (2014) Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environ Microbiol 16:467–485CrossRefGoogle Scholar
  31. Kosmala S, Karnkowska-Ishikawa A, Milanowski R, Kwiatowski J, Zakrys B (2009) Phylogeny and systematics of Euglena (Euglenaceae) species with axial, stellate chloroplasts based on morphological and molecular data-new taxa, emended diagnoses, and epitypifications. J Phycol 45:464–481CrossRefGoogle Scholar
  32. Kremp A, Tahvanainen P, Litaker W, Krock B, Suikkanen S, Leaw CP, Tomas C, De Clerck O (2014) Phylogenetic relationships, morphological variation, and toxin patterns in the Alexandrium ostenfeldii (Dinophyceae) complex: implications for species boundaries and identities. J Phycol 50:81–100CrossRefGoogle Scholar
  33. Kretschmann J, Zinßmeister C, Gottschling M (2014) Taxonomic clarification of the dinophyte Rhabdosphaera erinaceus Kamptner, ≡ Scrippsiella erinaceus comb. nov. (Thoracosphaeraceae, Peridiniales). Syst Biodivers 12:393–404CrossRefGoogle Scholar
  34. Kretschmann J, Elbrächter M, Zinßmeister C, Söhner S, Kirsch M, Kusber W-H, Gottschling M (2015a) Taxonomic clarification of the dinophyte Peridinium acuminatum Ehrenb., Scrippsiella acuminata, comb. nov. (Thoracosphaeraceae, Peridiniales). Phytotaxa 220:239–256CrossRefGoogle Scholar
  35. Kretschmann J, Filipowicz NH, Owsianny PM, Zinßmeister C, Gottschling M (2015b) Taxonomic clarification of the unusual dinophyte Gymnodinium limneticum Wolosz. (Gymnodiniaceae) from the Tatra Mountains. Protist 166:621–637CrossRefGoogle Scholar
  36. Krupnick GA, Kress WJ (2005) Plant conservation: a natural history approach. University of Chicago Press, ChicagoGoogle Scholar
  37. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS ONE 6:e29013CrossRefGoogle Scholar
  38. Langer MR, Weinmann AE, Lotters S, Bernhard JM, Rodder D (2013) Climate-driven range extension of Amphistegina (Protista, Foraminiferida): models of current and predicted future ranges. PLoS ONE 8: e54443CrossRefGoogle Scholar
  39. Le Bescot N, Mahé F, Audic S, Dimier C, Garet MJ, Poulain J, Wincker P, de Vargas C, Siano R (2016) Global patterns of pelagic dinoflagellate diversity across protist size classes unveiled by metabarcoding. Environ Microbiol 18:609–626CrossRefGoogle Scholar
  40. Lewis J (1991) Cyst-theca relationships in Scrippsiella (Dinophyceae) and related orthoperidinoid genera. Bot Mar 34:91–106Google Scholar
  41. Litaker RW, Vandersea MW, Kibler SR, Reece KS, Stokes NA, Lutzoni FM, Yonish BA, West MA, Black MND, Tester PA (2007) Recognizing dinoflagellate species using ITS rDNA sequences. J Phycol 43:344–355CrossRefGoogle Scholar
  42. Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112CrossRefGoogle Scholar
  43. Massana R, Gobet A, Audic S, Bass D, Bittner L et al. (2015) Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. Environ Microbiol 17:4035–4049CrossRefGoogle Scholar
  44. Matsuoka K, Cho HJ (2000) Morphological variation in cysts of the gymnodinialean dinoflagellate Polykrikos. Micropaleontology 46:360–364Google Scholar
  45. Mayer GC, Coyne JA, Losos JB, Foufopoulos J, Shubin N, Futuyma DJ, Campbell BC, Edwards SV (2013) Museums' role: increasing knowledge. Science 339:1148–1149CrossRefGoogle Scholar
  46. McCauley LAR, Erdner DL, Nagai S, Richlen ML, Anderson DM (2009) Biogeographic analysis of the globally distributed algal bloom species Alexandrium minutum (Dinophyceae) based on rRNA gene sequences and microsatellite markers. J Phycol 45:454–463CrossRefGoogle Scholar
  47. Milchakova NA, Phillips RC (2003) Black Sea seagrasses. Mar Pollut Bull 46:695–699CrossRefGoogle Scholar
  48. Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinopbyceae): evidence for cryptic species. Phycologia 42:56–70CrossRefGoogle Scholar
  49. Mullins J, Garofolo G, Van Ert M, Fasanella A, Lukhnova L, Hugh-Jones M, Blackburn J (2013) Ecological niche modeling of Bacillus anthracis on three continents: evidence for genetic-ecological divergence? PloS ONE 8: e72451Google Scholar
  50. Murray JW, Stewart K, Kassakian S, Krynytzky M, DiJulio D (2006) Oxic, suboxic and anoxic conditions in the Black Sea. In: Gilbert A, Yanko-Hombach V, Panin N (eds) Climate change and coastline migration as factors in human adaptation to the circum-pontic region: from past to forecast. Kluwer, New York, pp 437–452Google Scholar
  51. Osche G (1966) Die Welt der Parasiten. Zur Naturgeschichte des Schmarotzertums. Springer, BerlinCrossRefGoogle Scholar
  52. Ozsoy E, Di Iorio D, Gregg MC, Backhaus JO (2001) Mixing in the Bosphorus Strait and the Black Sea continental shelf: observations and a model of the dense water outflow. J Mar Syst 31:99–135CrossRefGoogle Scholar
  53. Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an indo-Pacific coral zooxanthella. Proc Natl Acad Sci U S A 112:7513–7518CrossRefGoogle Scholar
  54. Renner SS (2004) Plant dispersal across the tropical Atlantic by wind and sea currents. Int J Plant Sci Suppl 165:23–33CrossRefGoogle Scholar
  55. Rintala J-M, Hällfors H, Hällfors S, Hällfors G, Majaneva M, Blomster J (2010) Heterocapsa arctica subsp. frigida subsp. nov. (Peridiniales, Dinophyceae) – description of a new dinoflagellate and its occurrence in the Baltic Sea. J Phycol 46:751–762CrossRefGoogle Scholar
  56. Rocha LA, Aleixo A, Allen G, Almeda F, Baldwin CC et al. (2014) Specimen collection: an essential tool. Science 344:814–815CrossRefGoogle Scholar
  57. Said MA, Gerges MA, Maiyza IA, Hussein MA, Radwan AA (2011) Changes in Atlantic water characteristics in the south-eastern Mediterranean Sea as a result of natural and anthropogenic activities. Oceanologia 53:81–95CrossRefGoogle Scholar
  58. Smith SA, Donoghue MJ (2010) Combining historical biogeography with niche modeling in the Caprifolium clade of Lonicera (Caprifoliaceae, Dipsacales). Syst Biol 59:322–341CrossRefGoogle Scholar
  59. Söhner S, Zinßmeister C, Kirsch M, Gottschling M (2012) Who am I – and if so, how many? Species diversity of calcareous dinophytes (Thoracosphaeraceae, Peridiniales) in the Mediterranean Sea. Org Divers Evol 12:339–348CrossRefGoogle Scholar
  60. Soininen J (2012) Macroecology of unicellular organisms – patterns and processes. Environ Microbiol Rep 4:10–22CrossRefGoogle Scholar
  61. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K et al. (2015) Structure and function of the global ocean microbiome. Science 348:1261359CrossRefGoogle Scholar
  62. Tang YZ, Gobler CJ (2012) Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on eastern oyster (Crassostrea virginica) and northern quahog (Mercenaria mercenaria) larvae. Mar Biol 159:199–210CrossRefGoogle Scholar
  63. Tang YZ, Egerton TA, Kong L, Marshall HG (2008) Morphological variation and phylogenetic analysis of the dinoflagellate Gymnodinium aureolum from a tributary of Chesapeake Bay. J Eukaryot Microbiol 55:91–99CrossRefGoogle Scholar
  64. Taylor FJR (1980) On dinoflagellate evolution. BioSystems 13:65–108CrossRefGoogle Scholar
  65. Terenko L (2005) New dinoflagellate (Dinoflagellata) species from the Odessa Bay of the Black Sea. Oceanol Hydrobiol Stud 34 (Suppl 3):205–216Google Scholar
  66. Tsarenko PM, Vasser SP, Nevo E (2006) Algae of Ukraine: diversity, nomenclature, taxonomy, ecology and geography. Vol. 1. Cyanoprocaryota, Euglenophyta, Chrysophyta, Xanthophyta, Raphidophyta, Phaeophyta, Dinophyta, Cryptophyta, Glaucocystophyta, and Rhodophyta. Gantner, RuggelGoogle Scholar
  67. Vargas C, Audic S, Henry N, Decelle J, Mahé F et al. (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605CrossRefGoogle Scholar
  68. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206CrossRefGoogle Scholar
  69. Vink A (2004) Calcareous dinoflagellate cysts in south and equatorial Atlantic surface sediments: diversity, distribution, ecology and potential for palaeoenvironmental reconstruction. Mar Micropaleontol 50:43–88CrossRefGoogle Scholar
  70. Weiner A, Aurahs R, Kurasawa A, Kitazato H, Kucera M (2012) Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protists. Mol Ecol 21:4063–4073CrossRefGoogle Scholar
  71. Wu L, Sun Q, Sugawara H, Yang S, Zhou Y, McCluskey K, Vasilenko A, Suzuki K, Ohkuma M, Lee Y, Robert V, Ingsriswang S, Guissart F, Philippe D, Ma J (2013) Global catalogue of microorganisms (GCM): a comprehensive database and information retrieval, analysis, and visualization system for microbial resources. BMC Genomics 14:933CrossRefGoogle Scholar
  72. Zinßmeister C, Söhner S, Facher E, Kirsch M, Meier KJS, Gottschling M (2011) Catch me if you can: the taxonomic identity of Scrippsiella trochoidea (F.Stein) A.R.Loebl. (Thoracosphaeraceae, Dinophyceae). Syst Biodivers 9:145–157CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department Biologie, Systematische Botanik und MykologieGeoBio-Center, Ludwig-Maximilians-Universität MünchenMunichGermany
  2. 2.Department of Botany, School of Biology and ChemistryUniversity of OsnabrückOsnabrückGermany
  3. 3.Department of Biology and Pharmaceutical BotanyMedical University of GdańskGdańskPoland
  4. 4.Faculty of BiologyAlexandru Ioan Cuza University of IaşiIaşiRomania
  5. 5.NIRDBS/Stejarul Research Centre for Biological SciencesPiatra NeamţRomania
  6. 6.Universität Bremen, Fachbereich Geowissenschaften – Fachrichtung Historische Geologie/PaläontologieBremenGermany

Personalised recommendations