Abstract
A unique structural feature of diatoms is their hierarchically patterned siliceous cell wall. Silicon uptake, storage, and processing are necessary for the intracellular synthesis of these cell walls. Uptake occurs from the natural habitats, that is, salt-water or fresh-water reservoirs. Dissolved silicon is predominantly taken up as monosilicic acid, Si(OH)4. The required intracellular silicon concentrations are much higher than typical environmental concentrations. Therefore, stabilization and storage inside the cell are necessary. Silicic acid transporters (SITs) were identified and studied within the last decades. These proteins are found in all different diatom lineages. They are able to transport silicic acid into the cell interior. SITs are transmembrane proteins and work as silicic acid/sodium symporters. After silicic acid uptake, it must be stabilized against uncontrolled polycondensation and stored in the cell interior. Different models of silicon storage by diatoms are discussed. Moreover, the incorporation of different “foreign” inorganic elements, like iron or aluminum, in diatom biosilica occurs and can influence the structure. This chapter deals with the chemical transformation of silicic acid during uptake and transport before the start of cell wall silicification. Note that the molecular regulation of cell wall biosynthesis is the topic of another chapter.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- cDNA:
-
Complementary deoxyribonucleic acid
- cryo-FIB-SEM:
-
Cryo-focused ion beam scanning electron microscopy
- EDX:
-
Energy-dispersive X-ray spectroscopy
- EPR:
-
Electron paramagnetic resonance
- GXQ (X = Q, G, R, M):
-
Sequence motif (G: glycine, Q: glutamine, R: arginine, M: methionine)
- IR:
-
Infrared
- ITC:
-
Isothermal titration calorimetry
- K M :
-
Michaelis constant (in the Michaelis-Menten kinetics)
- MAS:
-
Magic angle spinning
- Men+:
-
Exchangeable counter ions like Na+, K+ or Ca2+
- mRNA:
-
Messenger ribonucleic acid
- NMR:
-
Nuclear magnetic resonance
- NP:
-
Nanoparticle
- Qn:
-
Si(OSi)n(OH)4−n moiety (n = 0, 1, 2, 3, 4)
- SIT:
-
Silicic acid transport protein
- SITL:
-
Diatom-like silicic acid transporters
- SDV:
-
Silicon deposition vesicle
- SSP:
-
Silicon storage pool
- STV:
-
Silicon transport vesicle
- V max :
-
Maximum reaction rate (in the Michaelis-Menten kinetics)
- [Si]:
-
Concentration of silicon
References
Annenkov VV, Basharina TN, Danilovtseva EN, Grachev MA (2013) Putative silicon transport vesicles in the cytoplasm of the diatom Synedra acus during surge uptake of silicon. Protoplasma 250:1147–1155. https://doi.org/10.1007/s00709-013-0495-x
Annenkov VV, Gordon R, Zelinskiy SN, Danilovtseva EN (2020) The probable mechanism for silicon capture by diatom algae: assimilation of polycarbonic acids with diatoms—is endocytosis a key stage in building of siliceous frustules? J Phycol 1737(1):1729–1737. https://doi.org/10.1111/jpy.13062
Azam F (1974) Silicic-acid uptake in diatoms studied with [68Ge]germanic acid as tracer. Planta 121:205–212. https://doi.org/10.1007/BF00389321
Azam F, Hemmingsen BB, Volcani BE (1973) Germanium incorporation into the silica of diatom cell walls. Arch Mikrobiol 92:11–20. https://doi.org/10.1007/BF00409507
Bhattacharyya P, Volcani BE (1980) Sodium-dependent silicate transport in the apochlorotic marine diatom Nitzschia alba. Proc Natl Acad Sci U S A 77:6386–6390. https://doi.org/10.1073/pnas.77.11.6386
Blank GS, Sullivan CW (1979) Diatom mineralization of silicic acid III. Si(OH)4 binding and light dependent transport in Nitzschia angularis. Arch Microbiol 123:157–164
Brembu T, Chauton MS, Winge P et al (2017) Dynamic responses to silicon in Thalasiossira pseudonana - identification, characterisation and classification of signature genes and their corresponding protein motifs. Sci Rep 7:1–14. https://doi.org/10.1038/s41598-017-04921-0
Brunner E, Gröger C, Lutz K et al (2009) Analytical studies of silica biomineralization: towards an understanding of silica processing by diatoms. Appl Microbiol Biotechnol 84:607–616. https://doi.org/10.1007/s00253-009-2140-3
Chisholm SW, Azam F, Eppley RW (1978) Silicic acid incorporation in marine diatoms on light: dark cycles: Use as an assay for phased cell division. Limnol Oceanogr 23:518–529. https://doi.org/10.4319/lo.1978.23.3.0518
Chou L, Wollast R (1997) Biogeochemical behavior and mass balance of dissolved aluminum in the western Mediterranean Sea. Deep Res Part II Top Stud Oceanogr 44:741–768. https://doi.org/10.1016/S0967-0645(96)00092-6
Conway HL, Harrison PJ, Davis CO (1976) Marine diatoms grown in chemostats under silicate or ammonium limitation. II. Transient response of Skeletonema costatum to a single addition of the limiting nutrient. Mar Biol 35:187–199. https://doi.org/10.1007/BF00390940
Conway HL, Harrison PJ, Davis CO (1977) Marine diatoms grown in chemostats under silicate or ammonium limitation. IV. Transient response of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida to a single addition of the limiting nutrient. Mar Biol 43:33–43. https://doi.org/10.1007/BF00390940
Coradin T, Eglin D, Livage J (2004) The silicomolybdic acid spectrophotometric method and its application to silicate/biopolymer interaction studies. Spectroscopy 18:567–576
Curnow P, Senior L, Knight MJ et al (2012) Expression, purification, and reconstitution of a diatom silicon transporter. Biochemistry 51:3776–3785. https://doi.org/10.1021/bi3000484
Davis AK, Hildebrand M (2008) A self-propagating system for Ge incorporation into nanostructured silica. Chem Commun:4495–4497. https://doi.org/10.1039/b804955f
Del Amo Y, Brzezinski MA (1999) The chemical form of dissolved Si taken up by marine diatoms. J Phycol 35:1162–1170. https://doi.org/10.1046/j.1529-8817.1999.3561162.x
Demadis KD, Brückner SI, Brunner E et al (2015) The intimate role of imidazole in the stabilization of silicic acid by a pH-responsive, histidine-grafted polyampholyte. Chem Mater 27:6827–6836. https://doi.org/10.1021/acs.chemmater.5b03100
Dixit S, Van Cappellen P, Van Bennekom AJ (2001) Processes controlling solubility of biogenic silica and pore water build-up of silicic acid in marine sediments. Mar Chem 73:333–352. https://doi.org/10.1016/S0304-4203(00)00118-3
Driscoll CT, Schecher WD (1990) The chemistry of aluminum in the environment. Environ Geochem Health 12:28–49. https://doi.org/10.1007/BF01734046
Durak GM, Taylor AR, Walker CE et al (2016) A role for diatom-like silicon transporters in calcifying coccolithophores. Nat Commun 7:10543. https://doi.org/10.1038/ncomms10543
Durkin CA, Koester JA, Bender SJ, Armbrust EV (2016) The evolution of silicon transporters in diatoms. J Phycol 52:716–731. https://doi.org/10.1111/jpy.12441
Ellwood MJ, Hunter KA (2000) The incorporation of zinc and iron into the frustule of the marine diatom Thalassiosira pseudonana. Limnol Oceanogr 45:1517–1524. https://doi.org/10.4319/lo.2000.45.7.1517
Encyclopedia Britannica. https://www.britannica.com/science/silicon. Accessed July 6, 2020
Gehlen M, Beck L, Calas G et al (2002) Unraveling the atomic structure of biogenic silica: evidence of the structural association of Al and Si in diatom frustules. Geochim Cosmochim Acta 66:1601–1609. https://doi.org/10.1016/S0016-7037(01)00877-8
Grachev MA, Bedoshvili YD, Gerasimov EY et al (2017) Silica-containing inclusions in the cytoplasm of diatom Synedra acus. Dokl Biochem Biophys 472:44–48. https://doi.org/10.1134/S1607672917010124
Gröger C, Sumper M, Brunner E (2008) Silicon uptake and metabolism of the marine diatom Thalassiosira pseudonana: Solid-state 29Si NMR and fluorescence microscopic studies. J Struct Biol 161:55–63. https://doi.org/10.1016/j.jsb.2007.09.010
Hildebrand M (2004) Silicic acid transport and its control during cell wall silicification in diatoms. In: Bäuerlein E (ed) Biomineralization: progress in biology, molecular biology and application. Wiley-VCH, Berlin, pp 159–176
Hildebrand M (2008) Diatoms, biomineralization processes, and genomics. Chem Rev 108:4855–4874
Hildebrand M, Volcani BE, Gassmann W, Schroeder JI (1997) A gene family of silicon transporters. Nature 385:688–689. https://doi.org/10.1111/mms.12107
Hildebrand M, Dahlin K, Volcani BE (1998) Characterization of a silicon transporter gene family in Cylindrotheca fusiformis: sequences, expression analysis, and identification of homologs in other diatoms. Mol Gen Genet 260:480–486. https://doi.org/10.1007/s004380050920
Holland HD (1984) The chemical evolution of the atmosphere and oceans. Princeton University Press, Princeton
Hydes DJ, de Lange GJ, de Baar HJW (1988) Dissolved aluminium in the Mediterranean. Geochim Cosmochim Acta 52:2107–2114. https://doi.org/10.1016/0016-7037(88)90190-1
Iler RK (1979) The chemistry of silica: solubility, polymerization, colloid and surface properties and biochemistry of silica. Wiley, New York, NY
Ingall ED, Diaz JM, Longo AF et al (2013) Role of biogenic silica in the removal of iron from the Antarctic seas. Nat Commun 4:1–6. https://doi.org/10.1038/ncomms2981
Jolles A, Neurath F (1898) Eine colorimetrische Methode zur Bestimmung der Kieselsäure im Wasser. Zeitschrift für Angew Chemie 11:315–316. https://doi.org/10.1002/ange.18980111403
Kaden J, Brückner SI, Machill S et al (2017) Iron incorporation in biosilica of the marine diatom Stephanopyxis turris: dispersed or clustered? Biometals 30:71–82. https://doi.org/10.1007/s10534-016-9987-4
Kinrade SD, Del Nin JW, Schach AS et al (1999) Stable five- and six-coordinated silicate anions in aqueous solution. Science (80-) 285:1542–1545. https://doi.org/10.1126/science.285.5433.1542
Kinrade SD, Gillson AME, Knight CTG (2002) Silicon-29 NMR evidence of a transient hexavalent silicon complex in the diatom Navicula pelliculosa. J Chem Soc Dalt Trans 3:307–309. https://doi.org/10.1039/b105379p
Knight MJ, Senior L, Nancolas B et al (2016) Direct evidence of the molecular basis for biological silicon transport. Nat Commun 7:1–11. https://doi.org/10.1038/ncomms11926
Köhler L, Machill S, Werner A et al (2017) Are diatoms ″green″ aluminosilicate synthesis microreactors for future catalyst production? Molecules 22:1–16. https://doi.org/10.3390/molecules22122232
Kumar S, Rechav K, Kaplan-Ashiri I, Gal A (2020) Imaging and quantifying homeostatic levels of intracellular silicon in diatoms. Sci Adv 6:eaaz7554. https://doi.org/10.1126/sciadv.aaz7554
Lewin JMC (1954) Silicon metabolism in diatoms I. Evidence for the role of reduced sulfur compounds in silicon utilization. J Gen Physiol 37:589–599
Lewin JMC (1955) Silicon metabolism in diatoms III. Respiration and silicon uptake in Navicula Pelliculosa. J Gen Physiol 39:1–10
Machill S, Kohler L, Ueberlein S et al (2013) Analytical studies on the incorporation of aluminium in the cell walls of the marine diatom Stephanopyxis turris. Biometals 26:141–150. https://doi.org/10.1007/s10534-012-9601-3
Marchetti A, Parker MS, Moccia LP et al (2009) Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457:467–470. https://doi.org/10.1038/nature07539
Marron AO, Ratcliffe S, Wheeler GL et al (2016) The evolution of silicon transport in eukaryotes. Mol Biol Evol 33:3226–3248. https://doi.org/10.1093/molbev/msw209
Martin-Jézéquel V, Hildebrand M, Brzezinski MA (2000) Silicon metabolism in diatoms: implications for growth. J Phycol 36:821–840. https://doi.org/10.1046/j.1529-8817.2000.00019.x
Measures CI, Edmond JM (1990) Aluminium in the south atlantic: steady state distribution of a short residence time element. Methods 95:5331–5340
Milligan AJ, Varela DE, Brzezinski MA, Morel FMM (2004) Dynamics of silicon metabolism and silicon isotopic discrimination in a marine diatom as a function of pCO2. Limnol Oceanogr 49:322–329. https://doi.org/10.4319/lo.2004.49.2.0322
Mock T, Samanta MP, Iverson V et al (2008) Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc Natl Acad Sci U S A 105:1579–1584. https://doi.org/10.1073/pnas.0707946105
Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:1–13. https://doi.org/10.3389/fmicb.2012.00043
Paasche E (1973) Silicon and the ecology of marine plankton diatoms. I. Thalassiosira pseudonana (Cyclotella nana) grown in a chemostat with silicate as limiting nutrient. Mar Biol 19:117–126. https://doi.org/10.1007/BF00353582
Pfeiffer-Laplaud M, Costa D, Tielens F et al (2015) Bimodal acidity at the amorphous silica/water interface. J Phys Chem C 119:27354–27362. https://doi.org/10.1021/acs.jpcc.5b02854
Preari M, Spinde K, Lazic J et al (2014) Bioinspired insights into silicic acid stabilization mechanisms: the dominant role of polyethylene glycol-induced hydrogen bonding. J Am Chem Soc 136:4236–4244. https://doi.org/10.1021/ja411822s
Qin T, Gutu T, Jiao J et al (2008) Biological fabrication of photoluminescent nanocomb structures by metabolic incorporation of germanium into the biosilica of the diatom Nitzschia frustulum. ACS Nano 2:1296–1304. https://doi.org/10.1021/nn800114q
Raven JA (1983) The transport and function of silicon in plants. Biol Rev 58:179–207. https://doi.org/10.1111/j.1469-185X.1983.tb00385.x
Ren JL, Zhang GL, Zhang J et al (2011) Distribution of dissolved aluminum in the Southern Yellow Sea: influences of a dust storm and the spring bloom. Mar Chem 125:69–81. https://doi.org/10.1016/j.marchem.2011.02.004
Rorrer GL, Chang CH, Liu SH et al (2005) Biosynthesis of silicon-germanium oxide nanocomposites by the marine diatom Nitzschia frustulum. J Nanosci Nanotechnol 5:41–49. https://doi.org/10.1166/jnn.2005.005
Sapriel G, Quinet M, Heijde M et al (2009) Genome-wide transcriptome analyses of silicon metabolism in Phaeodactylum tricornutum reveal the multilevel regulation of silicic acid transporters. PLoS One 4. https://doi.org/10.1371/journal.pone.0007458
Schmid AMM, Schulz D (1979) Wall morphogenesis in diatoms: deposition of silica by cytoplasmic vesicles. Protoplasma 100:267–288. https://doi.org/10.1007/BF01279316
Shrestha RP, Hildebrand M (2015) Evidence for a regulatory role of diatom silicon transporters in cellular silicon responses. Eukaryot Cell 14:29–40. https://doi.org/10.1128/EC.00209-14
Shrestha RP, Tesson B, Norden-Krichmar T et al (2012) Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana. BMC Genomics 13. https://doi.org/10.1186/1471-2164-13-499
Soleimani M, Rutten L, Maddala SP et al (2020) Modifying the thickness, pore size, and composition of diatom frustule in Pinnularia sp. with Al3+ ions. Sci Rep 10:19498. https://doi.org/10.1038/s41598-020-76318-5
Spinde K, Pachis K, Antonakaki I et al (2011) Influence of polyamines and related macromolecules on silicic acid polycondensation: relevance to “soluble silicon pools”? Chem Mater 23:4676–4687. https://doi.org/10.1021/cm201988g
Sullivan CW (1976) Diatom mineralization of silicic acid. I. Si(OH)4 transport characterisitcs in Navigula Pelliculosa. J Phycol 12:390–396
Sullivan CW (1977) Diatom mineralization of silicic acid. II. Regulation of Si(OH)4 transport rates during the cell cycle of Navicula Pelliculosa. J Phycol 13:86–91
Sullivan CW (1979) Diatom mineralization of silicic acid IV. Kinetics of soluble Si pool formation in exponentially growing and synchronized Navicula pelliculosa. J Phycol 15:210–216
Thamatrakoln K, Hildebrand M (2005) Approaches for functional characterization of diatom silicic acid transporters. J Nanosci Nanotechnol 5:158–166. https://doi.org/10.1166/jnn.2005.014
Thamatrakoln K, Hildebrand M (2007) Analysis of Thalassiosira pseudonana silicon transporters indicates distinct regulatory levels and transport activity through the cell cycle. Eukaryot Cell 6:271–279. https://doi.org/10.1128/EC.00235-06
Thamatrakoln K, Hildebrand M (2008) Silicon uptake in diatoms revisited: a model for saturable and nonsaturable uptake kinetics and the role of silicon transporters. Plant Physiol 146:1397–1407. https://doi.org/10.1104/pp.107.107094
Thamatrakoln K, Kustka AB (2009) When to say when: can excessive drinking explain silicon uptake in diatoms? BioEssays 31:322–327. https://doi.org/10.1002/bies.200800185
Thamatrakoln K, Alverson AJ, Hildebrand M (2006) Comparative sequence analysis of diatom silicon transporters: Toward a mechanistic model of silicon transport. J Phycol 42:822–834. https://doi.org/10.1111/j.1529-8817.2006.00233.x
Tréguer PJ, De La Rocha CL (2013) The world ocean silica cycle. Annu Rev Mar Sci 5:477–501. https://doi.org/10.1146/annurev-marine-121211-172346
Tréguer P, Pondaven P (2000) Silica control of carbon dioxide. Nature 406:358–359. https://doi.org/10.1093/bioinformatics/8.4.411
Tréguer P, Nelson DM, Van Bennekom AJ et al (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379. https://doi.org/10.1126/science.268.5209.375
Van Bennekom AJ, Buma AGJ, Nolting RF (1991) Dissolved aluminium in the Weddell-Scotia Confluence and effect of Al on the dissolution kinetics of biogenic silica. Mar Chem 35:423–434. https://doi.org/10.1016/S0304-4203(09)90034-2
Van Beusekom J, Weber A (1995) Der Einfluß von Aluminium auf das Wachstum und die Entwicklung von Kieselalgen in der Nordsee. Dtsch Hydrogr Zeitschrift Suppl 5:213–220
Vis BM, Wen J, Mellerup SK et al (2020) Silicon forms a rich diversity of aliphatic polyol complexes in aqueous solution. J Am Chem Soc 142:9188–9202. https://doi.org/10.1021/jacs.9b10701
Vrieling EG, Sun Q, Tian M et al (2007) Salinity-dependent diatom biosilicification implies an important role of external ionic strength. Proc Natl Acad Sci U S A 104:10441–10446. https://doi.org/10.1073/pnas.0608980104
Werner D (1966) Die Kieselsäure im Stoffwechsel von Cyclotella cryptica Reimann, Lewin und Guillard. Arch Mikrobiol 55:278–308. https://doi.org/10.1007/BF00410249
Acknowledgments
The authors wish to thank Prof. Nils Kröger (TU Dresden, Germany) for fruitful discussions. Thanks are further due to Prof. Kim Thamatrakoln (Rutgers University, New Brunswick, USA) and Dr. Assaf Gal (Weizmann Institute of Science, Rehovot, Israel) for their very helpful comments. Financial support from the DFG (FOR2038: Nanopatterned Organic Matrices in Biological Silica Mineralization, grant no. BR 1278/24-2) is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Kolbe, F., Brunner, E. (2022). Silicic Acid Uptake and Storage by Diatoms. In: Falciatore, A., Mock, T. (eds) The Molecular Life of Diatoms. Springer, Cham. https://doi.org/10.1007/978-3-030-92499-7_13
Download citation
DOI: https://doi.org/10.1007/978-3-030-92499-7_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-92498-0
Online ISBN: 978-3-030-92499-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)