Characterization of polyphosphate dynamics in the widespread freshwater diatom Achnanthidium minutissimum under varying phosphorus supplies.
Achnanthidium minutissimum
diatom
electron microscopy
phosphate uptake
polyphosphate
stimulated Raman scattering microscopy
Journal
Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935
Informations de publication
Date de publication:
01 Jan 2024
01 Jan 2024
Historique:
revised:
11
11
2023
received:
27
03
2023
accepted:
01
12
2023
medline:
2
1
2024
pubmed:
2
1
2024
entrez:
1
1
2024
Statut:
aheadofprint
Résumé
Polyphosphates (polyP) are ubiquitous biomolecules that play a multitude of physiological roles in many cells. We have studied the presence and role of polyP in a unicellular alga, the freshwater diatom Achnanthidium minutissimum. This diatom stores up to 2.0 pg·cell
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : GRK2272 (RTG R3)
Informations de copyright
© 2023 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.
Références
Aitchison, P., & Butt, V. (1973). The relation between the synthesis of inorganic polyphosphate and phosphate uptake by Chlorella vulgaris. Journal of Experimental Botany, 24, 497-510.
Alipanah, L., Winge, P., Rohloff, J., Najafi, J., Brembu, T., & Bones, A. M. (2018). Molecular adaptations to phosphorus deprivation and comparison with nitrogen deprivation responses in the diatom Phaeodactylum tricornutum. PLoS ONE, 13, e0193335.
Armbrust, E. V. (2009). The life of diatoms in the world's oceans. Nature, 459, 185-192.
Babes, V. (1895). Beobachtungen über die metachromatischen Körperchen, Sporenbildung, Verzweigung, Kolben-und Kapselbildung pathogener Bakterien. Zeitschrift für Hygiene und Infektionskrankheiten, 20(1), 412-437.
Bedoshvili, Y., Gneusheva, K., Popova, M., Morozov, A., & Likhoshway, Y. (2018). Anomalies in the valve morphogenesis of the centric diatom alga Aulacoseira islandica caused by microtubule inhibitors. Biology Open, 7(8), bio035519.
Benitez-Nelson, C. R. (2000). The biogeochemical cycling of phosphorus in marine systems. Earth Science Reviews, 51, 109-135.
Bondoc, K. G. V., Lembke, C., Vyverman, W., & Pohnert, G. (2019). Selective chemoattraction of the benthic diatom Seminavis robusta to phosphate but not to inorganic nitrogen sources contributes to biofilm structuring. Microbiology, 8, e00694.
Brown, M. R., & Kornberg, A. (2004). Inorganic polyphosphate in the origin and survival of species. Proceedings of the National Academy of Sciences of the United States of America, 101, 16085-16087.
Bru, S., Samper-Martin, B., Quandt, E., Hernandez-Ortega, S., Martinez-Lainez, J. M., Gari, E., Rafel, M., Torres-Torronteras, J., Marti, R., Ribeiro, M. P. C., Jimenez, J., & Clotet, J. (2017). Polyphosphate is a key factor for cell survival after DNA damage in eukaryotic cells. DNA Repair (Amst), 57, 171-178.
Caceres, C., Spatharis, S., Kaiserli, E., Smeti, E., Flowers, H., & Bonachela, J. A. (2019). Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake. The ISME Journal, 13, 2834-2845.
Cheng, J. X., & Xie, X. S. (2015). Vibrational spectroscopic imaging of living systems: An emerging platform for biology and medicine. Science, 350(6264), aaa8870.
Christ, J. J., & Blank, L. M. (2018). Enzymatic quantification and length determination of polyphosphate down to a chain length of two. Analytical Biochemistry, 548, 82-90.
De Jager, H. J., & Heyns, A. M. (1998). Study of the hydrolysis of sodium polyphosphate in water using Raman spectroscopy. Applied Spectroscopy, 52(6), 808-814.
Dell'Aquila, G., Zauner, S., Heimerl, T., Kahnt, J., Samel-Gondesen, V., Runge, S., Hempel, F., & Maier, U. G. (2020). Mobilization and cellular distribution of phosphate in the diatom Phaeodactylum tricornutum. Frontiers in Plant Science, 11, 579.
Diaz, J., Ingall, E., Benitez-Nelson, C., Paterson, D., de Jonge, M. D., McNulty, I., & Brandes, J. A. (2008). Marine polyphosphate: A key player in geologic phosphorus sequestration. Science, 320, 652-655.
Docampo, R., de Souza, W., Miranda, K., Rohloff, P., & Moreno, S. N. (2005). Acidocalcisomes - conserved from bacteria to man. Nature Reviews. Microbiology, 3, 251-261.
Dow, L. E. (2019). Interactions between the freshwater benthic diatom Achnanthidium minutissimum and the bacterium Dyadobacter sp. 32. [Doctoral dissertation, University of Konstanz, Germany].
Dyhrman, S. T., Jenkins, B. D., Rynearson, T. A., Saito, M. A., Mercier, M. L., Alexander, H., Whitney, L. P., Drzewianowski, A., Bulygin, V. V., Bertrand, E. M., Wu, Z., Benitez-Nelson, C., & Heithoff, A. (2012). The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS ONE, 7, e33768.
Eixler, S., Karsten, U., & Selig, U. (2006). Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply. Phycologia, 45(1), 53-60.
Falkner, G., & Falkner, R. (2011). The complex regulation of the phosphate uptake system of cyanobacteria. In G. Peschek, C. Obinger, & G. Renger (Eds.), Bioenergetic processes of cyanobacteria (pp. 109-130). Springer.
Fernando, E. Y., McIlroy, S. J., Nierychlo, M., Herbst, F. A., Petriglieri, F., Schmid, M. C., Wagner, M., Nielsen, J. L., & Nielsen, P. H. (2019). Resolving the individual contribution of key microbial populations to enhanced biological phosphorus removal with Raman-FISH. The ISME Journal, 13(8), 1933-1946.
Fisher, K. A. (1971). Polyphosphate in a chlorococcalean alga. Phycologia, 10, 177-182.
Guillard, R. R. (1975). Culture of phytoplankton for feeding marine invertebrates. In W. L. Smith & M. H. Chanley (Eds.), Culture of marine invertebrate animals: 1st conference on culture of marine invertebrate animal greenport (pp. 29-60). Springer.
Harold, F. (1964). Enzymic and genetic control of polyphosphate accumulation in Aerobacter aerogenes. Microbiology, 35, 81-90.
Hlúbiková, D., Ector, L., & Hoffmann, L. (2011). Examination of the type material of some diatom species related to Achnanthidium minutissimum (Kutz.) Czarn. (Bacillariophyceae). Algological Studies, 136-137, 19-43.
Hothorn, M., Neumann, H., Lenherr, E. D., Wehner, M., Rybin, V., Hassa, P. O., Uttenweiler, A., Reinhardt, M., Schmidt, A., Seiler, J., Ladurner, A. G., Herrmann, C., Scheffzek, K., & Mayer, A. (2009). Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science, 324, 513-516.
Huang, B., Marchand, J., Blanckaert, V., Lukomska, E., Ulmann, L., Wielgosz-Collin, G., Rabesaotra, V., Moreau, B., Bougaran, G., Mimouni, V., & Morant-Manceau, A. (2019). Nitrogen and phosphorus limitations induce carbon partitioning and membrane lipid remodelling in the marine diatom Phaeodactylum tricornutum. European Journal of Phycology, 54, 342-358.
Huang, W., Rio Bartulos, C., & Kroth, P. G. (2016). Diatom vacuolar 1,6-beta-transglycosylases can functionally complement the respective yeast mutants. The Journal of Eukaryotic Microbiology, 63, 536-546.
Hunter, J. E., Brandsma, J., Dymond, M. K., Koster, G., Moore, C. M., Postle, A. D., Mills, R. A., & Attard, G. S. (2018). Lipidomics of Thalassiosira pseudonana under phosphorus stress reveal underlying phospholipid substitution dynamics and novel diglycosylceramide substitutes. Applied and Environmental Microbiology, 84, e02034-17.
Kuhl, A. (1974). Phosphorus. In W. D. P. Stewart (Ed.), Algal physiology and biochemistry (pp. 636-654). Blackwell Scientific.
Lapointe, A., Spiteller, D., & Kroth, P. G. (2022). High throughput method for extracting polyphosphates from diatoms. Endocytosis and Cell Research, 31, 29-38.
Leitão, J. M., Lorenz, B., Bachinski, N., Wilhelm, C., Müller, W. E., & Schröder, H. C. (1995). Osmotic-stress-induced synthesis and degradation of inorganic polyphosphates in the alga Phaeodactylumtricornutum. Marine Ecology Progress Series, 121, 279-288.
Levasseur, M., Thompson, P. A., & Harrison, P. J. (1993). Physiological acclimation of marine phytoplankton to different nitrogen sources. Journal of Phycology, 29, 587-595.
Li, J., & Dittrich, M. (2019). Dynamic polyphosphate metabolism in cyanobacteria responding to phosphorus availability. Environmental Microbiology, 21, 572-583.
Li, J., Plouchart, D., Zastepa, A., & Dittrich, M. (2019). Picoplankton accumulate and recycle polyphosphate to support high primary productivity in coastal Lake Ontario. Scientific Reports, 9, 1-10.
Lieberman, L. (1890). Detection of metaphosphoric acid in the nuclein of yeast. Pflügers Archiv, 47, 155-160.
Lin, S., Litaker, R. W., & Sunda, W. G. (2016). Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. Journal of Phycology, 52, 10-36.
Liss, E., & Langen, P. (1962). Experiments on polyphosphate overcompensation in yeast cells after phosphate deficiency. Archiv für Mikrobiologie, 41, 383-392.
Mann, D. (1985). In vivo observations of plastid and cell division in raphid diatoms and their relevance to diatom systematics. Annals of Botany-London, 55, 95-108.
Martin, P., Dyhrman, S. T., Lomas, M. W., Poulton, N. J., & Van Mooy, B. A. (2014). Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proceedings of the National Academy of Sciences of the United States of America, 111, 8089-8094.
Martin, P., Van Mooy, B. A., Heithoff, A., & Dyhrman, S. T. (2011). Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana. The ISME Journal, 5, 1057-1060.
Meyer, A. (1904). Orientative studies on the distribution, morphology and chemistry of the volute. A. Felix.
Moudrikova, S., Sadowsky, A., Metzger, S., Nedbal, L., Mettler-Altmann, T., & Mojzes, P. (2017). Quantification of polyphosphate in microalgae by Raman microscopy and by a reference enzymatic assay. Analytical Chemistry, 89, 12006-12013.
Ogawa, N., DeRisi, J., & Brown, P. O. (2000). New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Molecular Biology of the Cell, 11, 4309-4321.
Paytan, A., & McLaughlin, K. (2007). The oceanic phosphorus cycle. Chemical Reviews, 107, 563-576.
Plouviez, M., Fernandez, E., Grossman, A. R., Sanz-Luque, E., Sells, M., Wheeler, D., & Guieysse, B. (2021). Responses of Chlamydomonas reinhardtii during the transition from P-deficient to P-sufficient growth (the P-overplus response): The roles of the vacuolar transport chaperones and polyphosphate synthesis. Journal of Phycology, 57, 988-1003.
Potapova, M., & Hamilton, P. B. (2007). Morphological and ecological variation within the Achnanthidium minutissimum (Bacillariophyceae) species complex. Journal of Phycology, 43, 561-575.
Rao, N. N., Gomez-Garcia, M. R., & Kornberg, A. (2009). Inorganic polyphosphate: Essential for growth and survival. Annual Review of Biochemistry, 78, 605-647.
Rao, N. N., Liu, S., & Kornberg, A. (1998). Inorganic polyphosphate in Escherichia coli: The phosphate regulon and the stringent response. Journal of Bacteriology, 180, 2186-2193.
Rashid, M. H., Rumbaugh, K., Passador, L., Davies, D. G., Hamood, A. N., Iglewski, B. H., & Kornberg, A. (2000). Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 97, 9636-9641.
Rhee, G. Y. (1973). A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. Journal of Phycology, 9, 495-506.
Rier, S. T., Kinek, K. C., Hay, S. E., & Francoeur, S. N. (2016). Polyphosphate plays a vital role in the phosphorus dynamics of stream periphyton. Freshwater Science, 35, 490-502.
Round, F. E. (2004). pH scaling and diatom distribution. Diatom, 20, 9-12.
Ruiz, F. A., Marchesini, N., Seufferheld, M., Govindjee, & Docampo, R. (2001). The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. The Journal of Biological Chemistry, 276, 46196-46203.
Sanz-Luque, E., Bhaya, D., & Grossman, A. R. (2020). Polyphosphate: A multifunctional metabolite in cyanobacteria and algae. Frontiers in Plant Science, 11, 938.
Schlösser, U. G. (1994). SAG-Sammlung von Algenkulturen at the University of Göttingen Catalogue of strains 1994. Botanica Acta: Journal of the German Botanical Society, 107, 113-186.
Schreiber, V., Dersch, J., Puzik, K., Bäcker, O., Liu, X., Stork, S., Schulz, J., Heimerl, T., Klingl, A., Zauner, S., & Maier, U. G. (2017). The central vacuole of the diatom Phaeodactylum tricornutum: Identification of new vacuolar membrane proteins and of a functional di-leucine-based targeting motif. Protist, 168(3), 271-282.
Secco, D., Wang, C., Shou, H., & Whelan, J. (2012). Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Letters, 586(4), 289-295.
Smith, S. A., & Morrissey, J. H. (2007). Sensitive fluorescence detection of polyphosphate in polyacrylamide gels using 4′,6-diamidino-2-phenylindol. Electrophoresis, 28, 3461-3465.
Smith, S. A., Wang, Y., & Morrissey, J. H. (2018). DNA ladders can be used to size polyphosphate resolved by polyacrylamide gel electrophoresis. Electrophoresis, 39, 2454-2459.
Solovchenko, A., Gorelova, O., Karpova, O., Selyakh, I., Semenova, L., Chivkunova, O., Baulina, O., Vinogradova, E., Pugacheva, T., Scherbakov, P., Vasilieva, S., Lukyanov, A., & Lobakova, E. (2020). Phosphorus feast and famine in cyanobacteria: Is luxury uptake of the nutrient just a consequence of acclimation to its shortage? Cell, 9, 1933.
Trilisenko, L., Kulakovskaya, E., & Kulakovskaya, T. (2017). The cadmim tolerance in Saccharomyces cerevisiae depends on inorganic polyphosphate. Journal of Basic Microbiology, 57, 982-986.
Van Mooy, B. A., Fredricks, H. F., Pedler, B. E., Dyhrman, S. T., Karl, D. M., Koblizek, M., Lomas, M. W., Mincer, T. J., Moore, L. R., Moutin, T., Rappe, M. S., & Webb, E. A. (2009). Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature, 458, 69-72.
Wiame, J. M. (1947). Study of a polyphosphorus, basophilic and metachromatic substance in yeasts. Biochimica et Biophysica Acta, 1, 234-255.
Windler, M. (2014). Bacterial influence on diatoms from photoautotrophic freshwater biofilms. [Doctoral dissertation, University of Konstanz, Germany].
Windler, M., Gruber, A., & Kroth, P. G. (2012). Purification of benthic diatoms from associated bacteria using the antibiotic imipenem. Endocytosis and Cell Research, 22, 62-65.
Xie, L., & Jakob, U. (2019). Inorganic polyphosphate, a multifunctional polyanionic protein scaffold. Journal of Biological Chemistry, 294(6), 2180-2190.
Yang, Z. K., Zheng, J. W., Niu, Y. F., Yang, W. D., Liu, J. S., & Li, H. Y. (2014). Systems-level analysis of the metabolic responses of the diatom Phaeodactylum tricornutum to phosphorus stress. Environmental Microbiology, 16, 1793-1807.
Yee, D. P., Hildebrand, M., & Tresguerres, M. (2020). Dynamic subcellular translocation of V-type H+-ATPase is essential for biomineralization of the diatom silica cell wall. The New Phytologist, 225(6), 2411-2422.
Yee, D. P., Samo, T. J., Abbriano, R. M., Shimasaki, B., Vernet, M., Mayali, X., Weber, P. K., Mitchell, B. G., Hildebrand, M., Decelle, J., & Tresguerres, M. (2023). The V-type ATPase enhances photosynthesis in marine phytoplankton and further links phagocytosis to symbiogenesis. Current Biology, 33, 2541-2547.