Skip to main content
Log in

Long-Term Temperature Acclimation of Photosynthesis in Steady-State Cultures of the Polar Diatom Fragilariopsis cylindrus

  • Regular paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Cultures of the obligate psychrophilic diatom Fragilariopsis cylindrus (Grunow) were grown for 4 months under steady-state conditions at −1 °C and +7 °C (50 μmol photons m−2 s−1) prior to measurements in order to investigate long-term acclimation of photosynthesis to both temperatures. No differences in maximum intrinsic quantum yield of PS II (FV/FM) and relative electron transport rates could be detected at either temperature after 4 months of acclimation. Measurements of photosynthesis (relative electron transport rates) vs. irradiance (P vs. E curves) revealed similar values for relative light utilization efficiency (α = 0.57 at −1 °C, α = 0.60 at +7 °C) but higher values for irradiance levels at which photosynthesis saturates (EK) at −1 °C and, therefore, higher maximum photosynthesis (PMAX = 54 (relative units) at −1 °C, PMAX = 49 at +7 °C). Nonphotochemical quenching (NPQ) measurements at 385 μmol photons m−2 s−1 indicated higher (37%) NPQ for diatoms grown at −1 °C compared to +7 °C, which was possibly related to a 2-fold increase in the concentration of the pigment diatoxanthin and a 9-fold up-regulation of a gene encoding a fucoxanthin chlorophyll a,c-binding protein. Expression of the D1 protein encoding gene psbA was ca. 1.5-fold up-regulated at −1 °C, whereas expression levels of other genes from Photosystem II (psbC, psbU, psbO), as well as rbcL, the gene encoding the Rubisco large subunit were similar at both temperatures. However, a 2-fold up-regulation of a plastid glyceraldehyde-P dehydrogenase at −1 °C indicated enhanced Calvin cycle activity. This study revealed for the first time that a polar diatom could efficiently acclimate photosynthesis over a wide range of polar temperatures given enough time. Acclimation of photosynthesis at −1 °C was probably regulated similarly to high light acclimation.

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.

Similar content being viewed by others

Abbreviations

α:

relative light utilization efficiency (ΔP/ΔE)

A, B, CCOMP:

amplitudes of fluorescence decay rate constants (K )

Chl:

chlorophyll

E :

irradiance (μmol photons m−2 s−1)

E K :

irradiance at the onset of light saturated photosynthesis

EST:

expressed sequence tag

ETR:

relative electron transport rate [(FV′/FM′) • PFD]

F 0 :

minimal Chl fluorescence in the dark

F M :

maximal Chl fluorescence in the dark

F M′ :

maximal Chl fluorescence during illumination

F t :

minimal Chl fluorescence during illumination

F V :

variable Chl fluorescence in the dark: (FMF0)

F V′ :

variable Chl fluorescence during illumination (FM′Ft)

FV/FM:

maximum potential quantum yield of PSII

FV′/FM’:

effective quantum yield of PSII

K A, B, C :

rate constant for fluorescence decay

K OPEN :

fraction of oxidized PSII RCs

JCON:

connectivity between PSII RCs

NPQ:

non photochemical quenching [(FMFM’)/FM′]

P:

photosynthesis (relative ETR)

PAR:

photosynthetically active radiation

PFD:

photon flux density (μmol photons m−2 s−1)

P MAX :

maximum photosynthetic rate (relative units)

PSII, I:

Photosystem II, I

PQ:

plastoquinone pool

PUFA:

polyunsaturated fatty acid

P vs. E:

photosynthesis versus irradiance

QA, B:

plastoquinone A, B

RC:

reaction centre

Rubisco:

ribulose-1,5-bisphosphate carboxylase

References

  • Z Adam AK Clarke (2002) ArticleTitleCutting edge of chloroplast proteolysis Trends Plant Sci 7 451–456 Occurrence Handle10.1016/S1360-1385(02)02326-9 Occurrence Handle12399180

    Article  PubMed  Google Scholar 

  • DJ Allen DR Ort (2001) ArticleTitleImpacts of chilling temperatures on warm-climate plants Trends Plant Sci 6 36–42 Occurrence Handle10.1016/S1360-1385(00)01808-2 Occurrence Handle11164376

    Article  PubMed  Google Scholar 

  • C Büchel C Wilhelm (1993) ArticleTitleIn vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives Photochem Photobiol 58 137–148

    Google Scholar 

  • BA Boczar AC Palmisano (1990) ArticleTitlePhotosynthetic pigments and pigment-proteins in natural populations of Antarctic sea ice diatoms Phycologia 29 470–477

    Google Scholar 

  • PW Boyd (2002) ArticleTitleEnvironmental factors controlling phytoplankton processes in the Southern Ocean J Phycol 38 844–861 Occurrence Handle10.1046/j.1529-8817.2002.t01-1-01203.x

    Article  Google Scholar 

  • GF Cota (1985) ArticleTitlePhotoadaptation of high Arctic ice algae Nature 315 219–222 Occurrence Handle10.1038/315219a0

    Article  Google Scholar 

  • IR Davison (1991) ArticleTitleEnvironmental effects on algal photosynthesis: temperature J Phycol 27 IssueID1 2–8 Occurrence Handle10.1111/j.0022-3646.1991.00002.x

    Article  Google Scholar 

  • N Devos M Ingouff R Loppes RF Matagne (1998) ArticleTitleRUBISCO adaptation to low temperatures: a comparative study in psychrophilic and mesophilic unicellular algae J Phycol 34 655–660 Occurrence Handle10.1046/j.1529-8817.1998.340655.x

    Article  Google Scholar 

  • PH Eilers JCH Peeters (1988) ArticleTitleA model for the relationship between light intensity and the rate of photosynthesis in phytoplankton Ecol Model 42 199–215 Occurrence Handle10.1016/0304-3800(88)90057-9

    Article  Google Scholar 

  • PG Falkowski J LaRoche (1991) ArticleTitleAcclimation to spectral irradiance in algae J Phycol 27 8–14 Occurrence Handle10.1111/j.0022-3646.1991.00008.x

    Article  Google Scholar 

  • M Fiala L Oriol (1990) ArticleTitleLight-temperature interactions on the growth of Antarctic diatoms Polar Biol 10 629–636

    Google Scholar 

  • B Genty JM Briantais NR Baker (1989) ArticleTitleThe relationship between the quantum yield of photosynthesis electron transport and quenching of chlorophyll fluorescence Biochim Biophys Acta 990 87–92

    Google Scholar 

  • F Gervais U Riebesell MY Gorbunov (2002) ArticleTitleChanges in primary productivity and chlorophyll a in response to iron fertilization in the Southern Polar Frontal Zone Limnol Oceanogr 47 1324–1335

    Google Scholar 

  • Gleitz M, Bartsch A, Dieckmann GS and Eicken H (1998).Composition and succession of sea ice diatom assemblages in the eastern and southern Weddell Sea, Antarctica. In: Lizotte MP and Arrigo KR (eds) pp 107–120. Washington, DC: American Geophysical Union

  • A Grunow (1884) ArticleTitleDiatomeen von Franz-Josef Land Denk Acad Wien 48 5–23

    Google Scholar 

  • RR Guillard JH Ryther (1962) ArticleTitleStudies on marine plankton diatoms. I. Cyclotella nana (Husted) and Detonula confervacea (Cleve) Can J Microbiol 8 229–239 Occurrence Handle13902807

    PubMed  Google Scholar 

  • P Halldal (1953) ArticleTitlePhytoplankton investigations from the weather ship M in the Norwegian Sea, 1948–49 Hvalradets Skr 38 1–91

    Google Scholar 

  • G Horvárth A Melis E Hildeg M Droppa L Vigh (1987) ArticleTitleRole of lipids in the organisation and function of Photosystem II studied by homogeneous catalytic hydrogenation of thylakoid membranes in situ Biochim Biophys Acta 891 68–74

    Google Scholar 

  • W Jiang L Fang M Inouye (1996) ArticleTitleComplete growth inhibition of Escherichia coli by ribosome trapping with truncated mRNA at low temperature Genes Cell 1 965–976 Occurrence Handle10.1046/j.1365-2443.1996.d01-219.x

    Article  Google Scholar 

  • BMA Kroon BB Prézelin (1995) ArticleTitleTemperature dependency of fluorescence decay parameters in an Antarctic isolate of the diatom Thalassiosira sp Antarct J US 159 160

    Google Scholar 

  • J Lavaud B Rousseau HJ Gorkom Particlevan AL Etienne (2002) ArticleTitleInfluence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum Plant Physiol 129 1398–1406 Occurrence Handle10.1104/pp.002014 Occurrence Handle12114593

    Article  PubMed  Google Scholar 

  • MP Lizotte CW Sullivan (1991) ArticleTitleRates of photoadaptation in sea ice diatoms from McMurdo Sound, Antarctica J Phycol 27 367–373 Occurrence Handle10.1111/j.0022-3646.1991.00367.x

    Article  Google Scholar 

  • MT Mardigan JM Martinko J Parker (1997) Brock – Biology of Microorganisms EditionNumber8 Prentice Hall International Inc New Jersey

    Google Scholar 

  • DP Maxwell S Falk CG Trick NPA Huner (1994) ArticleTitleGrowth at low temperature mimics high-light acclimation in Chlorella vulgaris Plant Physiol 105 535–543 Occurrence Handle12232221

    PubMed  Google Scholar 

  • K Maxwell NJ Johnson (2000) ArticleTitleChlorophyll Fluorescence – a Practical Guide J Exp Bot 51 659–668 Occurrence Handle10938857

    PubMed  Google Scholar 

  • T Mock BMA Kroon (2002) ArticleTitlePhotosynthetic energy conversion under extreme conditions – I: important role of lipids as structural modulators and energy sink under N-limited growth in Antarctic sea ice diatoms Phytochem 61 41–51 Occurrence Handle10.1016/S0031-9422(02)00216-9

    Article  Google Scholar 

  • T Mock K Valentin (2004) ArticleTitlePhotosynthesis and cold acclimation: molecular evidence from a polar diatom J Phycol 40 732–741 Occurrence Handle10.1111/j.1529-8817.2004.03224.x

    Article  Google Scholar 

  • RM Morgan-Kiss AG Ivanov J Williams M Kahn NPA Huner (2002a) ArticleTitleDifferential thermal effects on the energy distribution between Photosystem II and Photosystem I in thylakoid membranes of a psychrophilic and a mesophilic alga Biochim Biophys Acta 1561 251–265

    Google Scholar 

  • RM Morgan-Kiss AG Ivanov NPA Huner (2002b) ArticleTitleThe Antarctic psychrophile, Chlamydomonas subcaudata, is deficient in state I-state II transitions Planta 214 435–445 Occurrence Handle10.1007/s004250100635

    Article  Google Scholar 

  • A Neori Holm-Hansen (1982) ArticleTitleEffect of temperature on rate of photosynthesis in Antarctic phytoplankton Polar Biol 1 33–38 Occurrence Handle10.1007/BF00568752

    Article  Google Scholar 

  • A Oeltjen WE Krumbein E Riehl (2002) ArticleTitleInvestigations on transcript size, steady state mRNA concentrations and diurnal expression of genes encoding fucoxanthin chlorophyll a,c light harvesting polypeptides in the centric diatom Cyclotella cryptica Plant Biol 4 250–257 Occurrence Handle10.1055/s-2002-25737

    Article  Google Scholar 

  • T Pfannschmidt A Nilsson JF Allen (1999) ArticleTitlePhotosynthetic control of chloroplast gene expression Nature 397 625–628 Occurrence Handle10.1038/17624

    Article  Google Scholar 

  • MM Tilzer B Bodungen Particlevon V Smetacek (1985) Light-dependence of phytoplankton photosynthesis in the Antarctic Ocean: implications for regulating productivity WR Siegfried PR Condy RM Laws (Eds)   Springer Verlag Berlin 60–69

    Google Scholar 

  • MM Tilzer M Elbrächter WW Gieske B Beese (1986) ArticleTitleLight-temperature interactions in the control of photosynthesis in Antarctic phytoplankton Polar Biol 5 105–111 Occurrence Handle10.1007/BF00443382

    Article  Google Scholar 

  • MM Tilzer Z Dubinsky (1987) ArticleTitleEffects of temperature and day length on the mass balance of Antarctic phytoplankton Polar Biol 7 35–42 Occurrence Handle10.1007/BF00286822

    Article  Google Scholar 

  • M Trtilek DM Kramer M Koblizek L Nedbal (1997) ArticleTitleDual-modulation LED kinetik fluorometer J Lumin 72 597–599 Occurrence Handle10.1016/S0022-2313(97)00066-5

    Article  Google Scholar 

  • CH Quillfeld Particle Von (1997) ArticleTitleDistribution of diatoms in the Northeast Water Polynya, Greenland J Mar Syst 10 211–240 Occurrence Handle10.1016/S0924-7963(96)00056-5

    Article  Google Scholar 

  • SW Wright SW Jeffrey RFC Mantoura LA Llewellyn T Bjørnland D Repefa NA Welschmeyer (1991) ArticleTitleImproved HPLC method for the analysis of chlorophylls and caratenoids from marine phytoplankton Mar Ecol Prog Ser 77 183–196

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Mock.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mock, T., Hoch, N. Long-Term Temperature Acclimation of Photosynthesis in Steady-State Cultures of the Polar Diatom Fragilariopsis cylindrus. Photosynth Res 85, 307–317 (2005). https://doi.org/10.1007/s11120-005-5668-9

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-005-5668-9

Keywords

Navigation