Photoacclimation State of Thalassiosira weissflogii is not Affected by Changes in Optical Depth Under A Fluctuating Light Regime Simulating Deep Mixing

EK independence Thalassiosira weissflogii fluctuating light photoacclimation phytoplankton

Journal

Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935

Informations de publication

Date de publication:
08 2021
Historique:
revised: 26 01 2021
received: 30 10 2020
accepted: 28 01 2021
pubmed: 17 2 2021
medline: 25 2 2023
entrez: 16 2 2021
Statut: ppublish

Résumé

Satellite-based remote sensing allows for global estimates of phytoplankton primary productivity by converting measurements of ocean color or photon absorption into units of carbon fixation. Models which perform this conversion often require an estimate of phytoplankton photoacclimation state such as the carbon to chlorophyll a ratio (C:Chl). Recently, our group developed a new photoacclimation model that can be applied to models of primary production. The model assumes that the phytoplankton photoacclimation state is not affected by periods of darkness during deep mixing beneath the photic zone, due to reduction in the plastoquinone pool in darkness and the subsequent deactivation of the signal for chlorophyll synthesis. In this study, we tested these assumptions by culturing the marine diatom Thalassiosira weissflogii under fluctuating light conditions simulating three different optical depths with progressively increasing deep mixing periods. The photoacclimation state, measured by the ratio of C:Chl, in T. weissflogii was not affected by changes in the length of simulated deep mixing periods. In addition, analysis of photosynthesis vs. irradiance (PE) curves showed that increases in optical depth caused decreases in both the maximum Chl-normalized rate of photosynthesis (P

Identifiants

pubmed: 33590492
doi: 10.1111/jpy.13149
doi:

Substances chimiques

Chlorophyll 1406-65-1
Chlorophyll A YF5Q9EJC8Y

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1212-1222

Informations de copyright

© 2021 Phycological Society of America.

Références

Anning, T., MacIntyre, H., Pratt, S., Sammes, P., Gibb, S. & Geider, R. 2000. Photoacclimation in the marine diatom Skeletonema costatum. Limnol. Oceanogr. 45:1807-17.
Baker, N. 2008. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Bio. 59:89-113.
Baklouti, M., Diaz, F., Pinazo, C., Faure, V. & Queguiner, B. 2006. Investigation of mechanistic formulations depicting phytoplankton dynamics for models of marine pelagic ecosystems and description of a new model. Prog. Oceanogr. 71:1-33.
Ballieul, B., Berne, N., Murik, O., Petroutsos, D., Prihoda, J., Tanaka, A., Villanova, V. et al. 2015. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524:366-69.
Behrenfeld, M. & Falkowski, P. 1997. A consumer’s guide to phytoplankton primary productivity models. Limnol. Oceanogr. 42:1479-91.
Behrenfeld, M. & Kolber, Z. 1999. Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840-3.
Behrenfeld, M. & Milligan, A. 2013. Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5:217-46.
Behrenfeld, M., Boss, E., Siegel, D. & Shea, D. 2005. Carbon-based productivity and phytoplankton physiology from space. Global Biogeochem. Cy. 19:GB1006.
Behrenfeld, M., Halsey, K. & Milligan, A. 2008. Evolved physiological responses of phytoplankton to their integrated growth environment. Philo. Trans. B. Bio. Sci. 363:2687-2703.
Behrenfeld, M., O’Malley, R., Boss, E., Westberry, T., Graff, J., Halsey, K., Milligan, A., Siegel, D. & Brown, M. 2015. Revaluating ocean warming impacts on global phytoplankton. Nat. Clim. Change. 6:323-30.
Behrenfeld, M., Prasil, O., Babin, M. & Bruyant, F. 2004. In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. J. Phycol. 40:4-25.
Bollivar, D. 2006. Recent advances in chlorophyll biosynthesis. Photosyn. Res. 90:173-94.
Brown, M., Penta, W., Jones, B. & Behrenfeld, M. 2019. The ratio of single-turnover to multiple-turnover fluorescence varies predictably with growth rate and cellular chlorophyll in the green alga Dunaliella tertiolecta. Photosyn. Res. 140:65-76.
Chen, Y., Durnford, D., Koblizek, M. & Falkowski, P. 2004. Plastid regulation of Lhcb1 transcription in the Chlorophyte alga Dunaliella tertiolecta. Plant Physiol. 136:3737-50.
D’asaro, E. A. 2003. Performance of autonomous Lagrangian floats. J. Atmos. Ocean. Technol. 20:896-911.
Denman, K. & Gargett, A. 1983. Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnol. Oceanogr. 28:801-15.
Escoubas, J., Lomas, M., LaRoche, J. & Falkowski, P. 1995. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. USA 92:10237-41.
Falkowski, P. & LaRoche, J. 1991. Acclimation to spectral irradiance in algae. J. Phycol. 27:8-14.
Falkowski, P. & Owens, T. 1980. Light-shade adaptation. Two strategies in marine phytoplankton. Plant Physiol. 66:592-5.
Fietz, S. & Nicklisch, A. 2002. Acclimation of the diatom Stephanodiscus neoastraea and the cyanobacterium Planktothrix agardii to simulated natural light fluctuations. Photosyn. Res. 72:95-106.
Fisher, N. & Halsey, K. 2016. Mechanisms that increase the growth efficiency of diatoms in low light. Photosyn. Res. 129:183-97.
Frigerio, S., Campoli, C., Zorzan, S., Fantoni, L., Crosatti, C., Drepper, F., Heahnel, W., Cattivelli, L., Morosinotto, T. & Bassi, R. 2007. Photosynthetic antenna size in higher plants is controlled by the plastoquinone redox state at the post-transcriptional rather than transcriptional level. J. Biol. Chem. 282:P29457-69.
Fong, A. & Archibald, J. 2008. Evolutionary dynamics of light-independent protochlorophyllide oxidoreductase genes in the secondary plastids of cryptophyte algae. Eukaryot. Cell 7:550-3.
Halsey, K., Milligan, A. & Behrenfeld, M. 2010. Physiological optimization underlies growth rate-independent chlorophyll-specific gross and net primary production. Photosyn. Res. 103:125-37.
Halsey, K., O’Malley, R., Graff, J., Milligan, A. & Behrenfeld, M. 2013. A common partitioning strategy for photosynthetic products in evolutionarily distinct phytoplankton species. New Phytol. 198:1030-8.
Halsey, H., Milligan, A. & Behrenfeld, M. 2014. Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites 4:260-80.
Havelkova, H., Prasil, O. & Behrenfeld, M. 2004. Photoacclimation of Dunaliella tertiolecta (Chlorophyceae) under fluctuating irradiance. Photosynthetica 42:273-81.
Hunsperger, H., Randhawa, T. & Cattolico, R. 2015. Extensive horizontal gene transfer, duplication, and loss of chlorophyll synthesis genes in algae. BMC Evol. Biol. 15:16.
Ibelings, B., Kroon, B. & Mur, L. 1994. Acclimation of photosystem II in a cyanobacterium and a eukaryotic green alga to high and fluctuating photosynthetic photon flux densities, simulating light regimes induced by mixing in lakes. New Phytol. 128:407-24.
Jans, F., Mignolet, E., Houyoux, P. A., Cardol, P., Ghysels, B., Cuine, S., Cournac, L., Peltier, G., Remacle, C. & Franck, F. 2008. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinol reduction in the chloroplast of Chlamydomonas. Proc. Natl. Acad. Sci. USA 105:20546-551.
Jassby, A., & Platt, T. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21:540-7.
Kauss, D., Bischof, S., Steiner, S., Apel, K. & Meskauskiene, R. 2012. FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway. FEBS Lett. 586:211-6.
Kolber, Z., Prasil, O. & Falkowski, P. 1998. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim. Biophy. Acta. 1367:88-106.
Lee, Z., Carder, K., Marra, J., Steward, R. & Perry, M. 1996. Estimating primary productivity at depth from remote sensing. Appl. Opt. 35:463-74.
Lepetit, B., Strum, S., Rogato, A., Gruber, A., Sachse, M., Falciatore, A., Kroth, P. & Lavaud, J. 2013. High light acclimation in the secondary plastids containing diatom Phaeodactylum tricornutum is triggered by the redox state of the plastoquinone pool. Plant Physiol. 161:853-65.
Lewis, M. R. & Smith, J. C. 1983. A small volume, short incubation time method for measurement of photosynthesis as a function of incident irradiance. Mar. Ecol. Prog. Ser. 13:99-102.
Li, Z., Wakao, S., Fischer, B. & Niyogi, K. 2009. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60:239-60.
MacIntyre, H., Kana, T., Anning, T. & Geider, R. 2002. Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J. Phycol. 38:17-38.
Milligan, A., Aparicio, U. & Behrenfeld, M. 2012. Fluorescence and nonphotochemical quenching responses to simulated vertical mixing in the marine diatom Thalassiosira weissflogii. Mar. Ecol. Prog. Ser. 448:67-78.
Mills, M., Kropuenske, L., van Dijken, G., Alderkamp, A., Berg, G., Robinson, D., Welshmeyer, N. & Arrigo, K. 2010. Photophysiology in two southern ocean phytoplankton taxa: photosynthesis of Phaeocystis antarctica (Prymnesiophyceae) and Fragilariopsis cylindrus (Bacillariophyceae) under simulated mixed-layer irradiance. J. Phycol. 46:1114-27.
Moller, I. & Sweetlove, L. 2010. ROS signalling - specificity is required. Trends Plant Sci. 15:370-4.
Mullineaux, C. 2014. Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta. 1837:503-11.
Peltier, G. & Cournac, L. 2002. Chlororespiration. Ann. Rev. Plant. Biol. 53:523-550.
Pfannschmidt, T., Nilsson, A. & Allen, J. 1999. Photosynthetic control of chloroplast gene expression. Nature 397:625-8.
Pfannschmidt, T., Schutze, K., Brost, M. & Oelmuller, R. 2001. A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J. Biol. Chem. 276:36125-30.
Pfannschmidt, T. & Yang, C. 2012. The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses. Protoplasma 249:S125-36.
Prasil, O., Kolber, Z. & Falkowski, P. 2018. Control of the maximal chlorophyll fluorescence yield by the Qb binding site. Photosynthetica. 56:150-62.
Reinbothe, C., Bakkouri, M., Buhr, R., Muraki, N., Nomata, J., Kurisu, G., Fujita, Y. & Reinbothe, S. 2010. Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends Plant Sci. 15:614-24.
Richter, A., Peter, E., Lorenzen, S., Grimm, B. & Czarnecki, O. 2010. Rapid dark repression of 5-aminolevulinic acid synthesis in green barley leaves. Plant Cell Physiol. 51:670-81.
Ritchie, R. 2006. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosyn Res. 89:27-41.
Rochaix, J. 2011. Regulation of photosynthetic electron transport. Biochim. Biophys. Acta. 1870:375-83.
Shatwell, T., Nicklisch, A. & Kohler, J. 2012. Temperature and photoperiod effects on phytoplankton growing under simulated mixed layer light fluctuations. Limnol. Oceanogr. 57:541-53.
Siegel, D., Behrenfeld, M., Maritorena, S., McClain, C. R., Antione, D., Bailey, S. W., Bontempi, P. S. et al. 2013. Regional to global assessments of phytoplankton dynamics from the Sea WiFS mission. Remote Sens. Environ. 135:77-91.
Silsbe, G., Behrenfeld, M., Halsey, K., Milligan, A. & Westberry, T. 2016. The CAFE model: A net production model for global ocean phytoplankton. Global Biogeochem. Cy. 30:1756-77.
Smyth, T., Tilstone, G. & Groom, S. 2005. Integration of radiative transfer into satellite models of ocean primary productivity. J. Geophys. Res. 110:C10014.
Strand, A., Asami, T., Alonso, J., Ecker, J. & Chory, J. 2003. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421:79-83.
Suggett, D., Lefloch, E., Harris, G., Leonardos, N. & Geider, R. 2007. Different strategies of photoacclimation by two strains of Emiliana huxleyi (Haptophyta). J. Phycol. 43:1209-22.
Sukenik, A., Bennett, J. & Falkowski, P. 1987. Light-saturated photosynthesis - limitation by electron transport or carbon fixation. Biochim. Biophys. Acta. 891:205-15.
Tang, E. & Vincent, W. 2000. Effects of daylength and temperature on the growth and photosynthesis of an Arctic cyanobacterium, Schizothriz calcicole (Oscillatoriaceae). Eur. J. Phycol. 35:263-72.
Toth, S., Schansker, G. & Strasser, R. 2007. A non-invasive assay of the plastoquinone redox state based on the OJIP-transient. Photosyn. Res. 93:190-203.
Westberry, T., Behrenfeld, M., Siegel, M., Anning, T. & Geider, R. 2008. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Global Biogeochem. Cy. 22:GB2024.
Vandenhecke, J., Bastedo, J., Cockshutt, A., Campbell, D. & Huot, Y. 2015. Changes in the Rubisco to photosystem ratio dominates photoacclimation across phytoplankton taxa. Photosyn. Res. 124:275-91.
Van de Poll, W., Visser, R. & Buma, A. 2007. Acclimation to a dynamic irradiance regime changes excessive irradiance sensitivity of Emiliania huxleyi and Thalassiosira weisflogii. Limnol. Oceanogr. 52:1430-38.
Verity, P. 1981. Effects of temperature, irradiance and daylength on the marine diatom Leptocylindrus danicus Cleve. Photosynthesis and cellular composition. J. Exp. Mar. Biol. Ecol. 55:79-91.

Auteurs

Matthew Brown (M)

Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, 97331, USA.

Allen Milligan (A)

Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, 97331, USA.

Michael Behrenfeld (M)

Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, 97331, USA.

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