Skip to main content
SpringerLink
Log in

Searching for a Mate: Pheromone-Directed Movement of the Benthic Diatom Seminavis robusta

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Diatoms are species-rich microalgae that often have a unique life cycle with vegetative cell size reduction followed by size restoration through sexual reproduction of two mating types (MT+ and MT−). In the marine benthic diatom Seminavis robusta, mate-finding is mediated by an l-proline-derived diketopiperazine, a pheromone produced by the attracting mating type (MT−). Here, we investigate the movement patterns of cells of the opposite mating type (MT+) exposed to a pheromone gradient, using video monitoring and statistical modeling. We report that cells of the migrating mating type (MT+) respond to pheromone gradients by simultaneous chemotaxis and chemokinesis. Changes in movement behavior enable MT+ cells to locate the direction of the pheromone source and to maximize their encounter rate towards it.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Field CB, Behrenfeld MJ, Randerson JT et al (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  2. Yool A, Tyrrell T (2003) Role of diatoms in regulating the ocean’s silicon cycle. Global Biogeochem Cy 17, GB1103

    Article  Google Scholar 

  3. Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192

    Article  CAS  PubMed  Google Scholar 

  4. Sarthou G, Timmermans KR, Blain S et al (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42

    Article  CAS  Google Scholar 

  5. Chepurnov VA, Mann DG, Sabbe K et al (2004) Experimental studies on sexual reproduction in diatoms. Int Rev Cytol 237:91–154

    Article  CAS  PubMed  Google Scholar 

  6. von Dassow P, Montresor M (2010) Unveiling the mysteries of phytoplankton life cycles: patterns and opportunities behind complexity. J Plankton Res 33:3–12

    Article  Google Scholar 

  7. Frenkel J, Vyverman W, Pohnert G (2014) Pheromone signaling during sexual reproduction in algae. Plant J 79:632–644

    Article  CAS  PubMed  Google Scholar 

  8. Gillard J, Frenkel J, Devos V et al (2013) Metabolomics enables the structure elucidation of a diatom sex pheromone. Angew Chem Int Ed Engl 52:854–857

    Article  CAS  PubMed  Google Scholar 

  9. Sato S, Beakes G, Idei M et al (2011) Novel sex cells and evidence for sex pheromones in diatoms. PLoS One 6, e26923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev Camb Philos Soc 82:265–289

    Article  PubMed  Google Scholar 

  11. Edgar R, Drolet D, Ehrman JM et al (2014) Motile male gametes of the araphid diatom Tabularia fasciculata search randomly for mates. PLoS One 9, e101767

    Article  PubMed  PubMed Central  Google Scholar 

  12. Moeys S, Frenkel J, Lembke C et al (2016) A sex-inducing pheromone triggers cell cycle arrest and mate attraction in the diatom Seminavis robusta. Sci Rep 6:19252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang J, Cao S, Du C et al (2013) Underwater locomotion strategy by a benthic pennate diatom Navicula sp. Protoplasma 250:1203–1212

    Article  CAS  PubMed  Google Scholar 

  14. Cohn SA, Halpin D, Hawley N et al (2015) Comparative analysis of light-stimulated motility responses in three diatom species. Diatom Res 30:213–225

    Article  Google Scholar 

  15. Cooksey B, Cooksey KE (1988) Chemical signal-response in diatoms of the Genus Amphora. J Cell Sci 91:523–529

    CAS  Google Scholar 

  16. Bondoc KGV, Heuschele J, Gillard J et al (2016) Selective silicate-directed motility in diatoms. Nat Commun 7:10540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Maier I, Calenberg M (1994) Effect of Extracellular Ca2+ and Ca2+- antagonists on the movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Bot Acta 107:451–460

    Article  CAS  Google Scholar 

  18. Gillard J, Devos V, Huysman MJ et al (2008) Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta. Plant Physiol 148:1394–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Barbara GM, Mitchell JG (2003) Marine bacterial organisation around point-like sources of amino acids. FEMS Microbiol Ecol 43:99–109

    Article  CAS  PubMed  Google Scholar 

  20. Berg HC (1993) Random walks in biology. Princeton University Press, Princeton

    Google Scholar 

  21. Blackburn N, Fenchel T, Mitchell J (1998) Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282:2254–2256

    Article  CAS  PubMed  Google Scholar 

  22. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  CAS  PubMed  Google Scholar 

  23. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  24. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer Science & Business Media

  25. Pinheiro J, Bates D, DebRoy S et al (2015) _nlme: linear and nonlinear mixed effects models_. vol R package version 3.1-121

  26. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Roy Stat Soc B 73:3–36

    Article  Google Scholar 

  27. Fenchel T (2004) Orientation in two dimensions: chemosensory motile behaviour of Euplotes vannus. Eur J Protistol 40:49–55

    Article  Google Scholar 

  28. Visser AW, Kiorboe T (2006) Plankton motility patterns and encounter rates. Oecologia 148:538–546

    Article  PubMed  Google Scholar 

  29. Underwood GJC, Kromkamp J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93–153

    Article  CAS  Google Scholar 

  30. Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45:361–402

    Article  Google Scholar 

  31. Edlund MB, Stoermer EF (1997) Ecological, evolutionary, and systematic significance of diatom life histories. J Phycol 33:897–918

    Article  Google Scholar 

  32. Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  33. Frenkel J, Wess C, Vyverman W et al (2014) Chiral separation of a diketopiperazine pheromone from marine diatoms using supercritical fluid chromatography. J Chromatogr B Anal Technol Biomed Life Sci 951–952:58–61

    Article  Google Scholar 

  34. Amsler CD, Iken KB (2001) Chemokinesis and chemotaxis in marine bacteria and algae. In: McClintock J. B. BBJ (ed) Marine Chemical Ecology. CRC Press, p 413–430

  35. Maier I (1993) Gamete orientation and induction of gametogenesis by pheromones in algae and plants. Plant Cell Environ 16:891–907

    Article  CAS  Google Scholar 

  36. Scalco E, Stec K, Iudicone D et al (2014) The dynamics of sexual phase in the marine diatom Pseudo‐nitzschia multistriata (Bacillariophyceae). J Phycol 50:817–828

    Article  PubMed  Google Scholar 

  37. Garren M, Son K, Raina JB et al (2014) A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J 8:999–1007

    Article  CAS  PubMed  Google Scholar 

  38. Dusenbery DB (1997) Minimum size limit for useful locomotion by free-swimming microbes. Proc Natl Acad Sci 94:10949–10954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Dusenbery DB (2000) Selection for high gamete encounter rates explains the success of male and female mating types. J Theor Biol 202:1–10

    Article  CAS  PubMed  Google Scholar 

  40. Pohnert G, Boland W (2002) The oxylipin chemistry of attraction and defense in brown algae and diatoms. Nat Prod Rep 19:108–122

    Article  CAS  PubMed  Google Scholar 

  41. Boland W, Pohnert G, Maier I (1995) Pericyclic reactions in nature: spontaneous Cope rearrangement inactivates algae pheromones. Angew Chem Int Ed Engl 34:1602–1604

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft within the framework of the CRC 1127 ChemBioSys, the IMPRS Exploration of Ecological Interactions with Molecular and Chemical Techniques, the International Leibniz Research School for Microbial and Biomolecular Interactions, the Flemish Research foundation project TG.0374.11 N, and the Ugent research grants 01/04611 and BOF15/GOA/17.

Author information

Authors and Affiliations

  1. Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich-Schiller-Universität Jena, Lessingstrasse 8, D-07743, Jena, Germany

    Karen Grace V. Bondoc, Christine Lembke & Georg Pohnert

  2. Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, D-07745, Jena, Germany

    Karen Grace V. Bondoc & Georg Pohnert

  3. Laboratory of Protistology and Aquatic Ecology, Department of Biology, University Gent, Krijgslaan 281 S8, 9000, Ghent, Belgium

    Wim Vyverman

Authors
  1. Karen Grace V. Bondoc
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christine Lembke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wim Vyverman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Georg Pohnert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Georg Pohnert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 80 kb)

Movie S1

The movie shows the attraction and accumulation of Seminavis robusta MT+ cells towards the diproline-loaded bead. Cells repeatedly touch the bead as an attempt to pair. The movie was accelerated 50 times and the scale bar indicates 50 μm. (AVI 27603 kb)

Movie S2

The movie shows that a control bead did not induce any reaction from S. robusta MT+ cells. The movie was accelerated 50 times and the scale bar indicates 50 μm. (AVI 27112 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bondoc, K.G.V., Lembke, C., Vyverman, W. et al. Searching for a Mate: Pheromone-Directed Movement of the Benthic Diatom Seminavis robusta . Microb Ecol 72, 287–294 (2016). https://doi.org/10.1007/s00248-016-0796-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0796-7

Keywords

Search

Navigation