Skip to main content
Log in

Differences in chloroplast ultrastructure of Phaeocystis antarctica in low and high light

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Phaeocystis antarctica Karsten exhibits optical changes in pigment packaging during acclimation to drastically different light levels. Here, the three-dimensional morphological rearrangements are shown for two light conditions mimicking limiting and saturating conditions for photosynthesis. Cultures of P. antarctica were grown semi-continuously under light-limiting conditions for growth (14 μmol quanta m−2 s−1) and a light-saturating condition (259 μmol quanta m−2 s−1) for growth. Increased numbers of thylakoids were observed under the low light treatment. In contrast, there were less amounts of thylakoid stacking in each chloroplast under the high light treatment. Electron microscopic tomographic reconstructions illustrate the complexity of the chloroplast organelle where the thylakoids ‘interact’ with the pyrenoid and the chloroplast membrane. Highly complex characteristics, such as bi- and tri-furcations in the thylakoid stacks, were continuous throughout the chloroplast. Other organelles, such as the Golgi apparatus and dense vesicles that may potentially affect cellular scattering and absorption were also observed in both high and low light. These three dimensional thylakoid arrangements have profound implications for cellular photophysiology. They represent a new view of algal chloroplast structure, and provide a starting point for more accurate optical modeling studies.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson RA (1989) Absolute orientation of the flagellar apparatus of Hiberdia magna comb. nov. (Chrysophyceae). Nord J Bot 8:653–669

    Article  Google Scholar 

  • Arrigo KR, Robinson DH, Worthen DL, Dunbar RB, DiTullio GR, VanWoert M, Lizotte MP (1999) Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science 283:365–367

    Article  PubMed  CAS  Google Scholar 

  • Berner T, Wyman K, Falkowski PG (1989) Photoadaptation and the “package effect” in Dunaliella tertiolecta (Chlorophyceae). J Phycol 25:70–78

    Article  CAS  Google Scholar 

  • Coggan JS, Bartol TM, Esquenazi E, Stiles JR, Lamont S, Martone ME, Berg DK, Ellisman MH, Sejnowski TJ (2005) Evidence for ectopic neurotransmission at a neuronal synapse. Science 309:446–451

    Article  PubMed  CAS  Google Scholar 

  • Davidson AT, Marchant HJ (1994) The impact of ultraviolet radiation on Phaeocystis and selected species of Antarctic marine diatoms. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation and biological research in Antarctica. Antarctic research Series 62, American Geophysical Union, Washington, DC, pp 187–205

    Google Scholar 

  • Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell, Malden

    Google Scholar 

  • Fan GY, Peltier S, Lamont S, Dunkelberger DG, Burke BE, Ellisman MH (2000) Multiport-readout frame-transfer 5 megapixel CCD imaging system for TEM applications. Ultramicroscopy 84:75–84

    Article  PubMed  CAS  Google Scholar 

  • Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319–324

    Article  PubMed  CAS  Google Scholar 

  • Gibbs SP (1962) The ultrastructure of the pyrenoids of green algae. J Ultrastruct Res 7:262–272

    Article  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies on marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • He W, Cowin P, Stokes DL (2003) Untangling desmosomal knots with electron tomography. Science 302:109–113

    Article  PubMed  CAS  Google Scholar 

  • Karlson B, Potter D, Kuylenstierna M, Anderson RA (1996) Ultrastructure, pigment composition, and 18S rRNA gene sequence for Nannochloropsis granulata sp. Nov. (Monodopsidaceae, Eustigmatophyceae), a marine ultraplankter isolated from the Skagerrak, northeast Atlantic Ocean. Phycologia 35:253–260

    Article  Google Scholar 

  • Ladinsky MS, Kremer JR, Furcinitti RS, McIntosh JR, Howell KE (1994) HVEM tomography of the trans-Golgi network: structural insights and identification of a lace-like vesicle coat. J Cell Biol 127:29–38

    Article  PubMed  CAS  Google Scholar 

  • Lancelot C, Keller MD, Rousseau V, Smith Jr. WO, Mathot S (1998) Autoecology of the marine haptophyte Phaeocystis sp. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Berlin, New York, Springer

  • Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119–132

    PubMed  CAS  Google Scholar 

  • Luther P (1992) Sample shrinkage and radiation damage. In: Frank J (eds) Electron tomography. Plenum, New York pp 39–60

    Google Scholar 

  • Mannella CA, Marko M, Penczek P, Barnard D, Frank J (1994) The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc Res Tech 27:278–283

    Article  PubMed  CAS  Google Scholar 

  • Mannella CA, Buttle K, Rath BK, Marko M (1998) Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8:225–228

    PubMed  CAS  Google Scholar 

  • Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci 98:2399–2406

    Article  PubMed  CAS  Google Scholar 

  • Martone ME, Gupta A, Wong M, Qian X, Sosinsky G, Ludascher B, Ellisman MH (2002) A cell-centered database for electron tomographic data. J Struct Biol 138:145–155

    Article  PubMed  CAS  Google Scholar 

  • Martone ME, Zhang S, Gupta A, Qian X, He H, Price DL, Wong M, Santini S, Ellisman MH (2003) The cell-centered database: a database for multi-scale structural and protein localization data from light and electron microscopy. Neuroinformatics 1:379–395

    Article  PubMed  Google Scholar 

  • Martone ME, Gupta A, Ellisman MH (2004) E-neuroscience: challenges and triumphs in integrating distributed data from molecules to brains. Nat Neurosci 7:467–472

    Article  PubMed  CAS  Google Scholar 

  • Moisan TA, Olaizola M, Mitchell BG (1998) Xanthophyll cycling in Phaeocystis antarctica Karsten: changes in cellular fluorescence. Mar Ecol Prog Ser:169:113–121

    Article  Google Scholar 

  • Moisan TA, Mitchell BG (1999) Photophysiological Acclimation of Phaeocystis antarctica Karsten under light limitation. Limnol Oceanogr 44:247–258

    Article  Google Scholar 

  • Müller WH, Koster AJ, Humbel BM, Ziese U, Verkleij AJ, van Aelst AC, van der Krift TP, Montijn RC, Boekhout T (2000) Automated electron tomography of the septal pore cap in Rhizoctonia solani. J Struct Biol 131:10–18

    Article  PubMed  Google Scholar 

  • Neale PJ, Banaszak A, Jarriel CR (1998) Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J Phycol 34:928–938

    Article  CAS  Google Scholar 

  • O’Toole ET, Winey M, McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10:2017–2031

    PubMed  CAS  Google Scholar 

  • Palmisano AC, SooHoo JB, Sullivan CW (1987) Effects of four environmental variables on photosynthesis–irradiance relationships in Antarctic sea-ice microalgae. Mar Biol 94:299–306

    Article  Google Scholar 

  • Perkins GA, Renken CW, Song JY, Frey TG, Young SJ, Lamont S, Martone ME, Lindsey S, Ellisman MH (1997) Electron tomography of large, multicomponent biological structures. J Struct Biol 120:219–227

    Article  PubMed  CAS  Google Scholar 

  • Riegger L, Robinson D (1997) Photoinduction of UV-absorbing compounds in Antarctic diatoms and Phaeocystis antarctica. Mar Ecol Prog Ser 160:13–25

    Article  Google Scholar 

  • Smallen S, Cirne W, Frey J, Berman F, Wolski R, Su M-H Kesselman C, Young S, Ellisman M (2000) Combining workstations and supercomputers to support grid applications: the parallel tomography experience. In: Proceeding 9th Heterogenous Computing Workshop, IEEE Computer Society Press, May 1, 2000, Cancun, pp 241–252

  • Smith Jr. WO, Asper VL (2001) The influence of phytoplankton assemblage composition on biogeochemical characteristics and cycles in the southern Ross Sea, Antarctica. Deep-Sea Res I 48:137–161

    CAS  Google Scholar 

  • Soto GE, Young SJ, Martone ME, Deerinck TJ, Lamont SP, Carragher BO, Hama K, Ellisman MH (1994) Serial section electron tomography: a method for 3-D reconstruction of large structures. Neuroimage 1:230–243

    Article  PubMed  CAS  Google Scholar 

  • Trissel HW, Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18:415–419

    Article  Google Scholar 

  • van Boeckel WHM, Hansen FC, Riegman R, Bak R (1992) Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial food web. Mar Ecol Prog Ser 81:269–276

    Article  Google Scholar 

  • Vernet M, Brody EA, Holm-Hansen O, Mitchell BG (1994) The response of Antarctic phytoplankton to ultraviolet light: absorption, photosynthesis, and taxonomic composition. Antarct Res Ser 62:143–158

    Google Scholar 

Download references

Acknowledgments

We thank Steve Barlow for help with preparation of samples for EM, Ying Jones for assistance with sectioning as well as William Schmidt, Benjamin Philmus, Neil Bonsteel, and Rocco Greco for tracing of thylakoids. We thank Steve Lamont for help with computational methods and Maryanne Martone for many helpful and insightful discussions. We thank Piotr Flatau for many inspirational discussions. We especially thank the two reviewers for improving our manuscript. This work was supported by NASA grants 972-274-45-00-01 and 972-622-52-50-02 (TAM) and MCB 9728338, 0131425 (GES). This work was in part supported by a NASA Level I Congressional Milestone. We thank Richard Mitchell and Robert N. Swift for computer assistance. The electron tomography work described in this paper was conducted at the National Center for Microscopy and Imaging Research at San Diego, which is supported by National Institutes of Health Grant RR04050 awarded to M.H.E. The CCDB is supported by NIH Human Brain Project Grant DA016602.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiffany A. Moisan.

Additional information

Communicated by J.P. Grassle, New Brunswick

Electronic supplementary material

Appendix 1

Appendix 1

Supplemental on-line figure

Flowchart of methods used for electron tomography starting with preparation of cells for electron microscopy and ending with analysis of three-dimensional structures. Letters on images at top, right, and bottom correspond to steps in flowchart at left. See Materials and methods for more details

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moisan, T.A., Ellisman, M.H., Buitenhuys, C.W. et al. Differences in chloroplast ultrastructure of Phaeocystis antarctica in low and high light. Mar Biol 149, 1281–1290 (2006). https://doi.org/10.1007/s00227-006-0321-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0321-5

Keywords

Navigation