ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS OF CARBON ALLOCATION IN MARINE PHYTOPLANKTON AS A FUNCTION OF NITROGEN AVAILABILITY: A FOURIER TRANSFORM INFRARED SPECTROSCOPY APPROACH1: C ALLOCATION AS A FUNCTION OF N AVAILABILITY
Abstract
An imbalance in the cellular C:N ratio may appreciably affect C allocation in algal cells. The consequences of these rearrangements of cellular pools on cell energetics, ecological fitness, and evolutionary trajectories are little known, although they are expected to be substantial. We investigated the fate of C in 11 microalgae cultured semicontinuously at three [NO3 (-) ] and constant pCO2 . We developed a new computational method for the semiquantitative use of Fourier transform infrared (FTIR) spectroscopy data for the determination of macromolecular composition. No obvious relationship was observed between the taxonomy and the allocation strategies adopted by the 11 species considered in this study. Not all species responded to a lower N availability by accumulating lipids or carbohydrates: Dunaliella parva W. Lerche and Thalassiosira pseudonana Hasle et Heimdal were homeostatic with respect to organic cell composition. A hyperbolic dependence of the lipid concentration from cell volume was observed. The level of reduction of organic constituents of green algae was parabolically related to size and was modulated in response to changes in N availability; the same was not true for the species bearing a "red" chloroplast. The above observations are discussed with respect to phytoplankton species composition and palatability for grazers, oleogenesis, and overall cell energetics.
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Nutritional variability causes changes in the macromolecular composition of microalgae cells.
“Several studies to improve lipid production in microalgae have shown that nutritional variability causes changes in the macromolecular composition of microalgae cells [5,6].”
From Response to nutrient variation on lipid productivity in green microalgae captured using second derivative FTIR and Raman spectroscopy (2022) · cites this paper as [6]
Not all microalgae species respond to nutrient scarcity by accumulating carbohydrates or lipids.
“Although nutritional scarcity has caused metabolic changes in microalgae, such as the accumulation of carbohydrates and lipids, not all species have responded to nutrient scarcity by accumulating carbohydrates or lipids [6,13,14].”
From Response to nutrient variation on lipid productivity in green microalgae captured using second derivative FTIR and Raman spectroscopy (2022) · cites this paper as [6]
Cites
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
Colorimetric Method for Determination of Sugars and Related Substances
DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956) · Analytical Chemistry · doi:10.1021/ac60111a017 · Cited by 52,269 · see citing works
A simplification of the protein assay method of Lowry et al. which is more generally applicable
Peterson, G. L. (1977) · Analytical Biochemistry · doi:10.1016/0003-2697(77)90043-4 · Cited by 8,531 · see citing works
Elser, J. J., Bracken, M. E. S., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H., Ngai, J. T., Seabloom, E. W., Shurin, J. B., & Smith, J. E. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01113.x · Cited by 4,593 · see citing works
Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances
Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., & Darzins, A. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03492.x · Cited by 3,745 · see citing works
Evolution of Phosphorus Limitation in Lakes
Schindler, D. W. (1977) · Science · doi:10.1126/science.195.4275.260 · Cited by 2,622 · see citing works
Animal Physiology: Adaptation and Environment
Schmidt‐Nielsen, K. (1962) · Cited by 2,498 · see citing works
Redfield revisited: Variability of C:N: P in marine microalgae and its biochemical basis
Geider, R., & La Roche, J. (2002) · European Journal of Phycology · doi:10.1017/s0967026201003456 · Cited by 1,412 · see citing works
Falkowski, P. G. (1997) · Nature · doi:10.1038/387272a0 · Cited by 1,308 · see citing works
Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge?
Anbar, A. D., & Knoll, A. H. (2002) · Science · doi:10.1126/science.1069651 · Cited by 1,191 · see citing works
Animal Physiology: Adaptation and environment
Baggott, G. K. (1985) · Journal of Arid Environments · doi:10.1016/s0140-1963(18)31286-2 · Cited by 1,111 · see citing works
Lipids and lipid metabolism in eukaryotic algae
Guschina, I. A., & Harwood, J. L. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.01.001 · Cited by 1,110 · see citing works
STITT, M., & KRAPP, A. (1999) · Plant, Cell & Environment · doi:10.1046/j.1365-3040.1999.00386.x · Cited by 1,044 · see citing works
Phosphate Depletion in the Western North Atlantic Ocean
Wu, J., Sunda, W. G., Boyle, E. A., & Karl, D. M. (2000) · Science · doi:10.1126/science.289.5480.759 · Cited by 793 · see citing works
Berges, J. A., Franklin, D. J., & Harrison, P. J. H. (2001) · Journal of Phycology · doi:10.1046/j.1529-8817.2001.01052.x · Cited by 594 · see citing works
Dean, A. P., Sigee, D. C., Estrada, B., & Pittman, J. K. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.01.065 · Cited by 523 · see citing works
Shifrin, N. S., & Chisholm, S. W. (1981) · Journal of Phycology · doi:10.1111/j.1529-8817.1981.tb00865.x · Cited by 488 · see citing works
EFFECT OF NUTRIENT LIMITATION ON FATTY ACID AND LIPID CONTENT OF MARINE MICROALGAE1
Reitan, K. I., Rainuzzo, J. R., & Ôlsen, Y. (1994) · Journal of Phycology · doi:10.1111/j.0022-3646.1994.00972.x · Cited by 473 · see citing works
Developments in mid-infrared FT-IR spectroscopy of selected carbohydrates
Kačuráková, M. (2001) · Carbohydrate Polymers · doi:10.1016/s0144-8617(00)00245-9 · Cited by 470 · see citing works
Integration of Carbon and Nitrogen Metabolism in Plant and Algal Cells
Huppe, H. C., & Turpin, D. H. (1994) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.pp.45.060194.003045 · Cited by 462 · see citing works
Kroth, P. G., Chiovitti, A., Gruber, A., Martin-Jezequel, V., Mock, T., Parker, M. S., Stanley, M. S., Kaplan, A., Caron, L., Weber, T., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001426 · Cited by 439 · see citing works
Guillén, M. D., & Cabo, N. (1997) · Journal of the American Oil Chemists Society · doi:10.1007/s11746-997-0058-4 · Cited by 425 · see citing works
Energetics and Transport in Aquatic Plants
Raven, J. A. (1984) · Medical Entomology and Zoology · Cited by 385 · see citing works
Martin, T., Oswald, O., & Graham, I. A. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.010475 · Cited by 379 · see citing works
Rapid method for the determination of lipid from the green alga Botryococcus braunii
Lee, S. J., Yoon, B.-D., & Oh, H.-M. (1998) · Biotechnology Techniques · doi:10.1023/a:1008811716448 · Cited by 368 · see citing works
Stehfest, K., Toepel, J., & Wilhelm, C. (2005) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2005.07.001 · Cited by 316 · see citing works
Wilhelm, C., Büchel, C., Fisahn, J., Goss, R., Jakob, T., LaRoche, J., Lavaud, J., Lohr, M., Riebesell, U., Stehfest, K., et al. (2006) · Protist · doi:10.1016/j.protis.2006.02.003 · Cited by 312 · see citing works
Giordano, M., Kansiz, M., Heraud, P., Beardall, J., Wood, B., & McNaughton, D. (2001) · Journal of Phycology · doi:10.1046/j.1529-8817.2001.037002271.x · Cited by 301 · see citing works
Self-citationThe evolution of silicification in diatoms: inescapable sinking and sinking as escape?
Raven, J. A., & Waite, A. M. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01022.x · Cited by 285 · see citing works
Importance of the diazotrophs as a source of new nitrogen in the ocean
LaRoche, J., & Breitbarth, E. (2004) · Journal of Sea Research · doi:10.1016/j.seares.2004.05.005 · Cited by 284 · see citing works
Lipid composition of the nitrogen starved green alga Neochloris oleoabundans
Tornabene, T. G., Holzer, G., Lien, S., & Burris, N. (1983) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(83)90026-1 · Cited by 265 · see citing works
Evolution of primary producers in the sea
(2008) · Choice Reviews Online · doi:10.5860/choice.45-3183 · Cited by 263 · see citing works
Granum, E., Kirkvold, S., & Myklestad, S. M. (2002) · Marine Ecology Progress Series · doi:10.3354/meps242083 · Cited by 246 · see citing works
Evolutionary Trajectories and Biogeochemical Impacts of Marine Eukaryotic Phytoplankton
Katz, M. E., Finkel, Z. V., Grzebyk, D., Knoll, A. H., & Falkowski, P. G. (2004) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130137 · Cited by 238 · see citing works
FT-IR Microspectroscopy Enhances Biological and Ecological Analysis of Algae
Murdock, J. N., & Wetzel, D. L. (2009) · Applied Spectroscopy Reviews · doi:10.1080/05704920902907440 · Cited by 223 · see citing works
Lynn, S. G., Kilham, S. S., Kreeger, D. A., & Interlandi, S. J. (2000) · Journal of Phycology · doi:10.1046/j.1529-8817.2000.98251.x · Cited by 219 · see citing works
Beardall, J., & Giordano, M. (2002) · Australian Journal of Plant Physiology · doi:10.1071/pp01195 · Cited by 209 · see citing works
Self-citationNutritional Status and Diet Composition Affect the Value of Diatoms as Copepod Prey
Jones, R. H., & Flynn, K. J. (2005) · Science · doi:10.1126/science.1107767 · Cited by 191 · see citing works
Monitoring of biomass composition from microbiological sources by means of FT‐IR spectroscopy
Pistorius, A. M. A., DeGrip, W. J., & Egorova‐Zachernyuk, T. A. (2008) · Biotechnology and Bioengineering · doi:10.1002/bit.22220 · Cited by 177 · see citing works
Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae
GLASS, J. B., WOLFE‐SIMON, F., & ANBAR, A. D. (2009) · Geobiology · doi:10.1111/j.1472-4669.2009.00190.x · Cited by 174 · see citing works
Koski, M., Breteler, W. K., & Schogt, N. (1998) · Marine Ecology Progress Series · doi:10.3354/meps170169 · Cited by 159 · see citing works
Feeding selectivity and egg production of Calanus helgolandicus in the English Channel
Irigoien, X., Head, R. N., Harris, R., et al. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.1.0044 · Cited by 133 · see citing works
MICROALGAE AS A SOURCE OF FATTY ACIDS
BEHRENS, P. W., & Kyle, D. J. (1996) · Journal of Food Lipids · doi:10.1111/j.1745-4522.1996.tb00073.x · Cited by 131 · see citing works
Impact of osmolytes on buoyancy of marine phytoplankton
Boyd, C. E., & Gradmann, D. (2002) · Marine Biology · doi:10.1007/s00227-002-0872-z · Cited by 104 · see citing works
(2019) · CRC Press eBooks · doi:10.1201/9780429061639 · Cited by 95 · see citing works
Binder, B. J., & Anderson, D. M. (1990) · Journal of Phycology · doi:10.1111/j.0022-3646.1990.00289.x · Cited by 93 · see citing works
Jakob, T., Wagner, H., Stehfest, K., & Wilhelm, C. (2007) · Journal of Experimental Botany · doi:10.1093/jxb/erm084 · Cited by 89 · see citing works
The Animal-Plant Complex in Forage Palatability Phenomena
Marten, G. C. (1978) · Journal of Animal Science · doi:10.2527/jas1978.4651470x · Cited by 89 · see citing works
(2009) · Science Publishers eBooks · doi:10.1201/b10300 · Cited by 80 · see citing works
Giordano, M., & Bowes, G. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.115.3.1049 · Cited by 78 · see citing works
Self-citationDomenighini, A., & Giordano, M. (2009) · Journal of Phycology · doi:10.1111/j.1529-8817.2009.00662.x · Cited by 78 · see citing works
Self-citationYoung, E. B., & Beardall, J. (2003) · Journal of Phycology · doi:10.1046/j.1529-8817.2003.02109.x · Cited by 69 · see citing works
Otero, A., & Fábregas, J. (1997) · Aquaculture · doi:10.1016/s0044-8486(97)00214-7 · Cited by 59 · see citing works
Marchetti, A., Varela, D. E., Lance, V. P., Lance, V. P., Palmucci, M., Giordano, M., & Armbrust, E. V. (2009) · Limnology and Oceanography · doi:10.4319/lo.2010.55.1.0011 · Cited by 54 · see citing works
Self-citationLarson, T. R., & Rees, T. A. V. (1996) · Journal of Phycology · doi:10.1111/j.0022-3646.1996.00388.x · Cited by 48 · see citing works
Koski, M., Wichard, T., & Jónasdóttir, S. H. (2008) · Marine Biology · doi:10.1007/s00227-008-0965-4 · Cited by 46 · see citing works
Montechiaro, F., & Giordano, M. (2009) · Journal of Plant Physiology · doi:10.1016/j.jplph.2009.07.013 · Cited by 44 · see citing works
Self-citationFIXED CARBON PARTITIONING IN THE RED MICROALGA PORPHYRIDIUM SP. (RHODOPHYTA)
Li, S., Lellouche, J., Shabtai, Y., et al. (2001) · Journal of Phycology · doi:10.1046/j.1529-8817.2001.037002289.x · Cited by 41 · see citing works
Homeostasis of cell composition during prolonged darkness
Montechiaro, F., Hirschmugl, C. J., Raven, J. A., & Giordano, M. (2006) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2006.01593.x · Cited by 39 · see citing works
Self-citationCollén, P. N., Camitz, A., Hancock, R. D., Viola, R., & Pedersén, M. (2004) · Journal of Phycology · doi:10.1111/j.1529-8817.2004.02174.x · Cited by 35 · see citing works
The Origin and Early Evolution of Green Plants
O’Kelly, C. J. (2007) · Elsevier eBooks · doi:10.1016/b978-012370518-1/50014-x · Cited by 33 · see citing works
CELLULAR LOCATION OF STARCH SYNTHESIS AND EVOLUTIONARY ORIGIN OF STARCH GENES
Raven, J. A. (2005) · Journal of Phycology · doi:10.1111/j.1529-8817.2005.00157.x · Cited by 18 · see citing works
Giordano, M., Norici, A., Gilmour, D. J., & Raven, J. A. (2007) · Functional Plant Biology · doi:10.1071/fp07049 · Cited by 12 · see citing works
Self-citationSeasonal and diet changes in ultrastructure in the dinoflagellate Ceratium hirundinella
Chapman, D. V., Dodge, J. D., & HEANEY, S. I. (1985) · Journal of Plankton Research · doi:10.1093/plankt/7.2.263 · Cited by 7 · see citing works
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Meng, Y., Yao, C., Xue, S., & Yang, H. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2013.10.064 · Cited by 174 · see citing works
Mayers, J. J., Flynn, K. J., & Shields, R. J. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.08.133 · Cited by 179 · see citing works
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- Authors
- Palmucci, M., Ratti, S., & Giordano, M.
- Affiliations
- Marche Polytechnic University (IT)
- Corresponding author
- Giordano, Mario
- ORCID
- Giordano, Mario
- Venue
- Journal of Phycology
- Publisher
- Wiley
- Published
- 2011-03-21
- Volume
- 47
- Issue
- 2
- Pages
- 313-323
- ISSN
- 0022-3646 (ISSN-L)
- OpenAlex
- W1581807545
- Cited by
- 104
- References
- 64
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 5 · 2023: 2 · 2022: 6 · 2021: 8 · 2020: 7 · 2019: 5 · 2018: 5 · 2017: 10 · 2016: 14 · 2015: 4 · 2014: 9 · 2013: 9 · 2012: 7
- FWCI
- 6.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Phycology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Keywords
- carbon allocation, nitrogen availability, marine microalgae, C/N ratio, macromolecular composition, lipid accumulation, carbohydrate accumulation, Dunaliella parva, Thalassiosira pseudonana, FTIR spectroscopy, cell energetics, phytoplankton community structure, red algae
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