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, Volume 1, Issue 2, pp 79–90 | Cite as

Some Observations of Diatoms Under Turbulence

  • Stephen J. Clarson
  • Miriam Steinitz-Kannan
  • Siddharth V. Patwardhan
  • Ramamurthi Kannan
  • Ryan Hartig
  • Louis Schloesser
  • Douglas W. Hamilton
  • Jeffrey K. A. Fusaro
  • Ryan Beltz
Original Paper

Abstract

The effect of turbulence on several freshwater diatom taxa was investigated and our findings are described herein. We have compared diatom morphology in shallow natural systems that experience turbulence due to wind and in river/waterfall systems where turbulence is due to high flow rates. We have also introduced turbulence into diatom laboratory cultures by mechanical shaking and by forcing air into the media. In particular, we have studied diatoms in five independent environments or cultures: the freshwater diatoms Tabellaria and Eunotia in equatorial lakes experiencing extreme seasonal variability in depth; two freshwater diatom monocultures of Aulacoseira granulata var angustissima and Melosira varians in the laboratory; and a freshwater diatom community possessing equal amounts (by number) of elongated and non-elongated diatoms (mostly Nitzschia and mostly Cyclotella, respectively) in the laboratory. We have demonstrated the effect of turbulence on freshwater diatom frustule morphologies and, perhaps more importantly, the effect of turbulence on freshwater diatom species population after controlled perturbation of the organisms’ environment. It has been widely reported that symmetry is often preferred in biological evolution, however here we have observed a preference towards asymmetry for the survival of diatoms in the presence of environmental stress (in particular, turbulence). We also note that to date there have been no systematic attempts to manipulate diatom frustules using external stimuli. We therefore present a proof-of-concept study in order to demonstrate: (i) that diatom morphologies can be manipulated by controlled simple external triggers (chemical and physical) (ii) that population balance (i.e. natural selection) can be controlled via simple external triggers (chemical and physical). This approach could open up an entire new field of future studies wherein controlled environmental perturbations are used to manipulate the structure, form, growth and reproduction of biological species.

Keywords

Diatoms Biosilica Silica Turbulence Natural selection 

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References

  1. 1.
    Briggs A (1996) Victorian Things, The Folio Society. St Edmundsbury Press, Bury St Edmunds, England, pp 83–118Google Scholar
  2. 2.
    Darwin C as cited in Murawski DA (1999) Diatoms: Plants with a touch of glass. In: Biodiversity: The Fragile Web, National Geographic, 195(2):114–121Google Scholar
  3. 3.
    Darwin C (1859 & 1968) On the Origin of Species by Means of Natural Selection or The Preservation of Favoured Races in the Struggle for Life Charles Darwin, (Ed. by J. W. Burrow), Penguin Books, Harmondsworth, Middlesex, England [This particular edition of “The Origin from 1968 was the one that was studied by one of us (SJC) while reading for an undergraduate degree at the University of York in England. It is the edition that has been used in this work. The first edition was published by John Murray in 1859 in London in a run of a mere 1,250 copies—which sold out immediately].Google Scholar
  4. 4.
    Round FE, Crawford RM, Mann DG (1990) The Diatoms: Biology & Morphology of the Genera. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  5. 5.
    Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam N, Zhou S, Allen A, Apt KP, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Schnitzler Parker M, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86CrossRefGoogle Scholar
  6. 6.
    Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jézéquel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Schnitzler Parker M, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van de Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244CrossRefGoogle Scholar
  7. 7.
    Alverson AJ, Cannone JJ, Gutell R, Theriot EC (2006) The evolution of elongate shape in diatoms. J. Phycol. 42:655–668CrossRefGoogle Scholar
  8. 8.
    Schmid AM (1979) Influence of environmental factors on the development of the valve in diatoms. Protoplasma 99:99–115CrossRefGoogle Scholar
  9. 9.
    Feldt LE, Stoermer EF, Schelske CL (1973) Occurrence of morphologically abnormal Synedra populations in Lake Superior phytoplankton. Proc 16th Conf Great Lakes Res:34–39Google Scholar
  10. 10.
    Falaco EF, Bona G, Badino HL, Ector L (2009) Diatom teratological forms and environmental alterations: a review. Hydrobiologia 623:1–35CrossRefGoogle Scholar
  11. 11.
    Debenest T, Silvestre J, Coste M, Delmas F, Pinelli E (2008) Herbicide effects on freshwater benthic diatoms: induction of nucleus alterations and silica cell wall abnormalities. Aquatic Toxicology 88:188–194CrossRefGoogle Scholar
  12. 12.
    Tapia P (2008) Diatoms as bioindicators of pollution in the Mantaro River, Central Andes, Peru. Int J Environ Health 2:82–91CrossRefGoogle Scholar
  13. 13.
    Dickman DM (1998) Benthic marine diatom deformities associated with contaminated sediments in Hong Kong. Environ Int 24:749–759CrossRefGoogle Scholar
  14. 14.
    Dickman MD, Yang JR, Brindle ID (1990) Impacts of heavy metals on higher aquatic plant, diatom and benthic invertebrate communities in the Niagara River watershed near Welland, Ontario. Water Pollut Res J Can 25:131–159Google Scholar
  15. 15.
    Hildebrand M (2005) Prospects of manipulating diatom silica nanostructures. J Nanosci Nanotech: A Special Issue on Diatom Nanotechnology 5:146–157Google Scholar
  16. 16.
    Rapp RA (2004) Manipulating diatoms. Materials Today 7:13Google Scholar
  17. 17.
    Frigeri LG, Radabaugh TR, Haynes PA, Hildebrand M (2006) Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana — Insights into silica structure formation. Molec. Cell Proteomics 5:182–193CrossRefGoogle Scholar
  18. 18.
    Dixit SS, Smol JP, Kingston JC, Charles DF (1992) Diatoms: powerful indicators of environmental change. Environ Sci Technol 26:23–33CrossRefGoogle Scholar
  19. 19.
    Battarbee RW (1986) Diatom analysis. In: Bergund BE (ed) Handbook of Holocene Paleoecology and Paleohydrology. Wiley, New York, pp 527–571Google Scholar
  20. 20.
    Ruggiu D, Luglié A, Cattaneo A, Panzani P (1998) Paleoecological evidence for diatom response to metal pollution in Lake Orta (N. Italy). J Paleolimnol 20:333–345CrossRefGoogle Scholar
  21. 21.
    Colinvaux PA (1993) Ecology 2. John Wiley and Sons, New York, USAGoogle Scholar
  22. 22.
    Schultz ME (1971) Salinity-related polymorphism in the brackish-water diatom Cyclotella cryptica. Can. J. Bot. 49:1285–1289CrossRefGoogle Scholar
  23. 23.
    Tuchman ML, Theriot EC, Stoermer EF (1984) Effects of low-level salinity concentrations on the growth of Cyclotella meneghiniana. Kütz Archiv Protistenkunde 128:319–326Google Scholar
  24. 24.
    Steinitz-Kannan M (2005) Effects of the environment on morphology of the silica cell wall in freshwater diatoms. Polymer Preprints 46(1):27Google Scholar
  25. 25.
    Steinitz-Kannan M (2009), Unpublished results.Google Scholar
  26. 26.
    Riedinger MA (1993) Doctoral Dissertation. The Ohio State University, Columbus, Ohio, USAGoogle Scholar
  27. 27.
    Vrieling EG, Beelen TPM, van Santen RA, Gieskes WWC (2000) Nanoscale uniformity of pore architecture in diatomaceous silica: a combined small and wide angle x-ray scattering study. J. Phycol. 36:146CrossRefGoogle Scholar
  28. 28.
    Stoermer EF (1967) Polymorphism in Mastogloia. J. Phycol. 3:73–77CrossRefGoogle Scholar
  29. 29.
    Paasche E (1975) An effect of osmotic pressure on the valve morphology of the diatom Skeletonema subsalsum (A. Cleve) Bethge. Phycologia 14:205–211Google Scholar
  30. 30.
    Margalef R (1997) Turbulence and marine life. Sci. Mar. 61(Suppl.1):109–123Google Scholar
  31. 31.
    Estrada M, Berdalet E (1997) Phytoplankton in a turbulent world. Sci. Mar. 61(Suppl.1):125–140Google Scholar
  32. 32.
    Gibson CH (1999) Fossil turbulence revisited. J Mar Syst 21:147–167CrossRefGoogle Scholar
  33. 33.
    Gibson, CH (2003) Turbulence and Diffusion: Fossil Turbulence (MS 138). Encyclopaedia of Ocean Sciences 1–12Google Scholar
  34. 34.
    Thomas, WH, Tynan, CT, Gibson, CH (1997) Turbulence-phytoplankton interrelationships. In: Round, F.E., Chapman, D.J. (Eds), Progress in Phycological Research 12, pp 283–324, Chap 5Google Scholar
  35. 35.
    Ruiz JD, Macias JD, Peters F (2004) Turbulence increases the average settling velocity of phytoplankton cells. Proc Natl Acad Sci 101:17720–17724CrossRefGoogle Scholar
  36. 36.
    Koehl MAR, Jumas PA, Karp-Boss L (2003) Algal biophysics. In: Norton TA (ed) Out of the Past. British Phycological Association, Belfast, Northern Ireland, pp 115–130Google Scholar
  37. 37.
    Pahlow M, Riebesell U, Wolf-Gladrow DA (1997) Impact of cell shape and chain formation on nutrient acquisition by marine diatoms Limnol. Oceanogr. 42:1660–1672Google Scholar
  38. 38.
    Visser A, Jonsson PR PR (2000) On the reorientation of non-spherical prey particles in a feeding current. J. of Plankton Res. 22:761–777CrossRefGoogle Scholar
  39. 39.
    Gomez NJ, Riera JL, Sabater S (1995) Ecology and morphological variability of Aulacoseira granulata (Bacillarophyceae) in Spanish reservoirs. J. Plankton. Res. 17:1–16CrossRefGoogle Scholar
  40. 40.
    Zirbel FV, Latz MI (2000) The reversible effect of flow on the morphology of Ceratocorys horrida (Peridiniales, dinophyta). J. Phycol. 36:46–58CrossRefGoogle Scholar
  41. 41.
    Billiones RG, Tackx ML, Daro MH (1999) The geometric features, shape factors and fractal dimensions of suspended particulate matter in the Scheldt Estuary (Belgium). Estuar Coast Shelf Sci 48:293–305CrossRefGoogle Scholar
  42. 42.
    Steinitz-Kannan M, Colinvaux PA, Kannan R (1983) Limnological studies in Ecuador: 1. Arch Hydrobiol 65:61–105Google Scholar
  43. 43.
    De Oliveira PE, Steinitz-Kannan M (1992) The diatom flora (Bacillariophyceae) of the Cuyabeno Faunistic Reserve, Ecuadorian Amazonia. Nova Hedwigia 54:515–552Google Scholar
  44. 44.
    Czarnecki DB (1987) The freshwater diatom culture collection at Loras College, Dubuque, Iowa. Notulae Naturae, Acad. Nat. Sci. Philadelphia. No. 465, pp.1–16Google Scholar
  45. 45.
    Anderson RA (2005) Algal Culturing Techniques. Academic, Elsevier, AmsterdamGoogle Scholar
  46. 46.
    Sommer U (1988) Growth and survival strategies of plankton diatoms. In: Sandgren CD (ed) Growth and Reproductive Strategies of Freshwater Phytoplankton. Cambridge University Press, Cambridge, England, pp 227–261Google Scholar
  47. 47.
    Hildebrand M, Doktycz M, Allison D (2008) Application of AFM in understanding biomineral formation in diatoms. Pflugers Arch. Eur. J. Physiol. 456:127–137CrossRefGoogle Scholar
  48. 48.
    Sherman BS, Webster IT (1998) Transitions between Aulacoseira and Anabaena dominance in a turbid river weeir pool. Limnol. Oceanogr. 43:1902–1915Google Scholar
  49. 49.
    Reynods CS (1994) The role of fluid motion in the dyanamics of phytoplankton in lakes and rivers. In: Giller PS, Hildrew AG, Raffaelli DG (eds) Aquatic Ecology. Scale, Pattern and Process. British Ecological Society. Blackwell Science, Oxford, England, pp 141–187Google Scholar
  50. 50.
    Hondzo M, Wuest A (2009) Do microscopic organisms feel turbulent flow? Environ Sci Technol 43:764–768CrossRefGoogle Scholar
  51. 51.
    Peters F, Marrase C (2000) Effects of turbulence on plankton: an overview of experimental evidence and some theoretical considerations. Mar Ecol- Prog Ser 205:291CrossRefGoogle Scholar
  52. 52.
    Peters F, Arin L, Marrase C, Berdalet E, Sala MM (2006) Effects of small-scale turbulence on the growth of two diatoms of different size in a phosphorus-limited medium. J Mar Syst 61:134–148Google Scholar
  53. 53.
    Hildebrand M, Wetherbee R (2003) Components and control of silicification in diatoms. Prog Mol Subcell Biol 33:11–57Google Scholar
  54. 54.
    Lopez PJ, Gautier C, Livage J, Coradin T (2005) Mimicking biogenic silica nanostructures formation. Current Nanoscience 1:73–83CrossRefGoogle Scholar
  55. 55.
    Brutchey RL, Morse DE (2008) Silicatein and the translation of its molecular mechanism of biosilicification into low temperature nanomaterial synthesis. Chem Rev 108:4915–4934CrossRefGoogle Scholar
  56. 56.
    Patwardhan SV, Mukherjee N, Clarson SJ (2001) Formation of fiber-like amorphous silica structures by externally applied shear. J. Inorg. Organomet. Polym. 11:117–121CrossRefGoogle Scholar
  57. 57.
    Patwardhan SV, Mukherjee N, Steinitz-Kannan M, Clarson SJ (2003) Bioinspired synthesis of new silica structures. Chem. Commun. 10:1122–1123CrossRefGoogle Scholar
  58. 58.
    Patwardhan SV, Clarson SJ, Perry CC (2005) On the role(s) of additives in bioinspired silicification. Chem. Comm. 9:1113–1121CrossRefGoogle Scholar
  59. 59.
    Beltz R, Clarson SJ, Hamilton DW, Steinitz-Kannan M, Patwardhan SV (2006) Effect of flow on the structure of biological and synthetic minerals. Polymer Preprints 47(2):1116Google Scholar
  60. 60.
    Davis AK, Hildebrand M, Palenik B (2005) Stress-induced protein associated with the girdle band region of the diatom Thalassiosira pseudonana (bacillariophyta). J. Phycol. 41:577–587CrossRefGoogle Scholar
  61. 61.
    Rodriguez F, Glawe DD, Naik RR, Hallinan KP, Stone MO (2004) Study of the chemical and physical influences upon in vitro peptide-mediated silica formation. Biomacromolecules 5:261–265CrossRefGoogle Scholar
  62. 62.
    Brott LL, Pikas DJ, Naik RR, Kirkpatrick SM, Tomlin DW, Whitlock PW, Clarson SJ, Stone MO (2001) Ultrafast holographic nanopatterning of biocatalytically-formed silica. Nature 413:291–293CrossRefGoogle Scholar
  63. 63.
    Naik RR, Brott LL, Clarson SJ, Stone MO (2002) Silica-precipitating peptides isolated from a combinatorial phage display peptide library. Journal of Nanoscience and Nanotechnology 2:95–100CrossRefGoogle Scholar
  64. 64.
    Naik RR, Whitlock PW, Rodriguez F, Brott LL, Glawe DD, Clarson SJ, Stone MO (2003) Controlled formation of biosilica structures in vitro. Chem. Comm. 238–239Google Scholar
  65. 65.
    Brott LL, Naik RR, Kirkpatrick SM, Whitlock PW, Clarson SJ, Stone MO (2005) Bioinspired organic-inorganic hybrid devices. In: Miziolek AW, Karna SP, Mauro JW, Vaia RA (eds) Defense Applications of Nanomaterials. American Chemical Society Symposium Series 891, Washington, DC, USA, pp 132–138CrossRefGoogle Scholar
  66. 66.
    Whitlock PW, Patwardhan SV, Stone MO, Clarson SJ (2008) Synthetic peptides derived from the diatom Cylindrotheca fusiformis: Kinetics of silica formation and morphological characterisation. In: Cheng HN, Gross RA (eds) Polymer Biocatalysis and Biomaterials 2. American Chemical Society Symposium Series 999, Washington, DC, USA, pp 412–433CrossRefGoogle Scholar
  67. 67.
    Thompson DW (1942) On Growth and Form. Cambridge University Press, Cambridge, England, pp 227–261Google Scholar
  68. 68.
    Jung C (1964) Man and His Symbols. Doubleday, New YorkGoogle Scholar

Copyright information

© Springer Science & Business Media BV 2009

Authors and Affiliations

  • Stephen J. Clarson
    • 1
  • Miriam Steinitz-Kannan
    • 2
  • Siddharth V. Patwardhan
    • 3
  • Ramamurthi Kannan
    • 4
  • Ryan Hartig
    • 2
  • Louis Schloesser
    • 2
  • Douglas W. Hamilton
    • 2
  • Jeffrey K. A. Fusaro
    • 5
  • Ryan Beltz
    • 1
  1. 1.Department of Chemical and Materials EngineeringUniversity of CincinnatiCincinnatiUSA
  2. 2.Department of Biological ScienceNorthern Kentucky UniversityHighland HeightsUSA
  3. 3.School of Biomedical and Natural SciencesNottingham Trent UniversityNottinghamUK
  4. 4.AFRLWright-Patterson Air Force BaseDaytonUSA
  5. 5.AGC Automotive AmericasHebronUSA

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