Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguilar M, Lado C (2012) Ecological niche models reveal the importance of climate variability for the biogeography of protosteloid amoebae. ISME J 6:1506–1514

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 8:737–745

    Article  PubMed  Google Scholar 

  • 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 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakan G, Büyükgüngör H (2000) The Black Sea. Mar Pollut Bull 41:24–43

    Article  CAS  Google Scholar 

  • Boenigk J, Ereshefsky M, Hoef-Emden K, Mallet J, Bass D (2012) Concepts in protistology: species definitions and boundaries. Eur J Protistol 48:96–102

    Article  PubMed  Google Scholar 

  • Caron DA (2009) Past president's address: Protistan biogeography: why all the fuss? J Eukaryot Microbiol 56:105–112

    Article  PubMed  Google Scholar 

  • 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 107:14679–14684

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 33:1317–1324

    Article  Google Scholar 

  • 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 57:1289–1303

    Article  Google Scholar 

  • 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 121:54–69

    Article  CAS  Google Scholar 

  • 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 160:386–396

    Article  PubMed  Google Scholar 

  • Fenchel T (2005) Cosmopolitan microbes and their ‘cryptic’ species. Aquat Microb Ecol 41:49–54

    Article  Google Scholar 

  • Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL (1993) A classification of living and fossil dinoflagellates. Micropaleontol Spec Publ:1–245

  • Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Environ Microbiol 296:1061–1063

    CAS  Google Scholar 

  • Foissner W (2007) Dispersal and biogeography of protists: recent advances. Jpn J Protozool 40:1–16

    Google Scholar 

  • 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 28:509–516

    Article  PubMed  Google Scholar 

  • Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK (2012) Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol 27:47–56

    Article  PubMed  Google Scholar 

  • 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 144:4975–4980

    Article  CAS  Google Scholar 

  • Gómez F, Boicenco L (2004) An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia 517:43–59

    Article  Google Scholar 

  • 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

  • Gottschling M, Kirsch M (2009) Annotated list of Scandinavian calcareous dinoflagellates collected in fall 2003. Berl Paläobiol Abh 10:193–198

    Google Scholar 

  • 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 40:207–220

    Article  CAS  Google Scholar 

  • 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 163:15–24

    Article  PubMed  Google Scholar 

  • 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 164:583–597

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61

    Google Scholar 

  • 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 14:1067–1084

    Article  Google Scholar 

  • 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 61:823–834

    Article  PubMed  Google Scholar 

  • Janofske D (2000) Scrippsiella trochoidea and Scrippsiella regalis, nov. comb. (Peridiniales, Dinophyceae): a comparison. J Phycol 36:178–189

    Article  Google Scholar 

  • 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 165:779–804

    Article  PubMed  PubMed Central  Google Scholar 

  • Kohli GS, Neilan BA, Brown MV, Hoppenrath M, Murray SA (2014) Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environ Microbiol 16:467–485

    Article  CAS  PubMed  Google Scholar 

  • 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 45:464–481

    Article  CAS  PubMed  Google Scholar 

  • 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 50:81–100

    Article  CAS  PubMed  Google Scholar 

  • Kretschmann J, Zinßmeister C, Gottschling M (2014) Taxonomic clarification of the dinophyte Rhabdosphaera erinaceus Kamptner, ≡ Scrippsiella erinaceus comb. nov. (Thoracosphaeraceae, Peridiniales). Syst Biodivers 12:393–404

    Article  Google Scholar 

  • 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 220:239–256

    Article  Google Scholar 

  • 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 166:621–637

    Article  PubMed  Google Scholar 

  • Krupnick GA, Kress WJ (2005) Plant conservation: a natural history approach. University of Chicago Press, Chicago

    Google Scholar 

  • 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:e29013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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: e54443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:609–626

    Article  CAS  PubMed  Google Scholar 

  • Lewis J (1991) Cyst-theca relationships in Scrippsiella (Dinophyceae) and related orthoperidinoid genera. Bot Mar 34:91–106

    Google Scholar 

  • 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 43:344–355

    Article  CAS  Google Scholar 

  • Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  PubMed  Google Scholar 

  • 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 17:4035–4049

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka K, Cho HJ (2000) Morphological variation in cysts of the gymnodinialean dinoflagellate Polykrikos. Micropaleontology 46:360–364

    Google Scholar 

  • Mayer GC, Coyne JA, Losos JB, Foufopoulos J, Shubin N, Futuyma DJ, Campbell BC, Edwards SV (2013) Museums' role: increasing knowledge. Science 339:1148–1149

    Article  CAS  PubMed  Google Scholar 

  • 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 45:454–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milchakova NA, Phillips RC (2003) Black Sea seagrasses. Mar Pollut Bull 46:695–699

    Article  CAS  PubMed  Google Scholar 

  • Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinopbyceae): evidence for cryptic species. Phycologia 42:56–70

    Article  Google Scholar 

  • 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: e72451

  • 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 437–452

    Google Scholar 

  • Osche G (1966) Die Welt der Parasiten. Zur Naturgeschichte des Schmarotzertums. Springer, Berlin

    Book  Google Scholar 

  • 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 31:99–135

    Article  Google Scholar 

  • 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 112:7513–7518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renner SS (2004) Plant dispersal across the tropical Atlantic by wind and sea currents. Int J Plant Sci Suppl 165:23–33

    Article  Google Scholar 

  • 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 46:751–762

    Article  CAS  Google Scholar 

  • Rocha LA, Aleixo A, Allen G, Almeda F, Baldwin CC et al. (2014) Specimen collection: an essential tool. Science 344:814–815

    Article  CAS  PubMed  Google Scholar 

  • 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 53:81–95

    Article  Google Scholar 

  • Smith SA, Donoghue MJ (2010) Combining historical biogeography with niche modeling in the Caprifolium clade of Lonicera (Caprifoliaceae, Dipsacales). Syst Biol 59:322–341

    Article  PubMed  Google Scholar 

  • 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 12:339–348

    Article  Google Scholar 

  • Soininen J (2012) Macroecology of unicellular organisms – patterns and processes. Environ Microbiol Rep 4:10–22

    Article  PubMed  Google Scholar 

  • Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K et al. (2015) Structure and function of the global ocean microbiome. Science 348:1261359

    Article  CAS  PubMed  Google Scholar 

  • 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 159:199–210

    Article  Google Scholar 

  • 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 55:91–99

    Article  PubMed  Google Scholar 

  • Taylor FJR (1980) On dinoflagellate evolution. BioSystems 13:65–108

    Article  CAS  PubMed  Google Scholar 

  • Terenko L (2005) New dinoflagellate (Dinoflagellata) species from the Odessa Bay of the Black Sea. Oceanol Hydrobiol Stud 34 (Suppl 3):205–216

    Google Scholar 

  • 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, Ruggel

  • Vargas C, Audic S, Henry N, Decelle J, Mahé F et al. (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605

    Article  CAS  PubMed  Google Scholar 

  • Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206

    Article  PubMed  Google Scholar 

  • Vink A (2004) Calcareous dinoflagellate cysts in south and equatorial Atlantic surface sediments: diversity, distribution, ecology and potential for palaeoenvironmental reconstruction. Mar Micropaleontol 50:43–88

    Article  Google Scholar 

  • 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 21:4063–4073

    Article  PubMed  Google Scholar 

  • 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 14:933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:145–157

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marc Gottschling.

Ethics declarations

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).

Additional information

Communicated by B. Beszteri

Electronic supplementary material

ESM 1

(PDF 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Žerdoner Čalasan, A., Kretschmann, J., Filipowicz, N.H. et al. Towards global distribution maps of unicellular organisms such as calcareous dinophytes based on DNA sequence information. Mar Biodiv 49, 749–758 (2019). https://doi.org/10.1007/s12526-018-0848-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-018-0848-y

Keywords

Navigation