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Electron-opaque microscopic fibrils in lakes: Their demonstration, their biological derivation and their potential significance in the redistribution of cations

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Summary

In lakes, the non-living particulate and the colloidal organic component are usually much greater in mass than the living component. Electron microscopy reveals that electron-opaque, non-rigid fibrils of approximately 3 to 10 nm diameter are found abundantly on the surfaces of common lake algae and microbes, free in the water column and free on the surface of the lake bottom. Filtration experiments and some microscopical evidence indicate that these fibrils are readily lost by cells without concomitant cell damage. Individual fibrils may form complex meshlike aggregates which can break apart and reassociate. Meshlike aggregates also appear to adhere to cells and large suspended particles. The behaviour and contact relations of the fibrils and their aggregates suggest a role in contact cation exchange. This suggested role is bolstered by a composition of 20 to 30 percent uronic acid residues for washed samples from lake water. Water from axenic algal cultures and from lakes can be processed by a combination of filtration and centrifugation techniques to yield quantities of purified fibril preparations permitting chemical analyses. Initial analyses show some of their physical characteristics to be appropriate to the principal component of an hypothetical, organic, carrier system for the redistribution of bound but biologically available cations in lakes.

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References

  • Allen, M. M., 1968: Ultrastructure of the cell wall and cell division of unicellular blue-green algae. J. Bacteriol.96, 842–852.

    PubMed  Google Scholar 

  • Aminoff, D., W. W. Binkley, R. Schaffer, andR. W. Mowry, 1970: Analytical methods for carbohydrates. In: The carbohydrates, second edition, Volume 2 B (Pigman, W., andD. Horton, eds.). New York: Academic Press.

    Google Scholar 

  • Bishop, C. T., G. A. Adams, andE. O. Hughes, 1954: A polysaccharide from the blue-green algaAnabaena cylindrica. Canad. J. Chem.32, 999–1004.

    Google Scholar 

  • Bitter, T., andH. M. Muir, 1962: A modified uronic acid carbazole reaction. Anal. Biochem.4, 330–334.

    PubMed  Google Scholar 

  • Brown, D. L., A. Massalski, andG. G. Leppard, 1976: Fine structure of excystment of the quadriflagellate algaPolytomella agilis. Protoplasma90, 155–171.

    PubMed  Google Scholar 

  • Cagle, G. D., 1975: Fine structure and distribution of extracellular polymer surrounding selected aerobic bacteria. Canad. J. Microbiol.21, 395–408.

    Google Scholar 

  • —,R. M. Pfister, andG. R. Vela, 1972: Improved staining of extracellular polymer for electron microscopy: examination ofAzotobacter, Zoogloea, Leuconostoc, andBacillus. Appl. Microbiol.24, 477–487.

    PubMed  Google Scholar 

  • Charlton, M. N., 1975: Sedimentation: measurements in experimental enclosures. Verh. Internat. Verein. Limnol.19, 267–272.

    Google Scholar 

  • Chu, S. P., 1942: The influence of the mineral composition of the medium on the growth of planktonic algae. J. Ecol.30, 284–325.

    Google Scholar 

  • Colvin, J. R., andG. G. Leppard, 1973: Fibrillar, modified polygalacturonic acid in, on and between plant cell walls. In: Biogenesis of plant cell wall polysaccharides (Loewus, F., ed.). New York: Academic Press.

    Google Scholar 

  • Dodge, J. D., 1974: Fine structure and phylogeny in the algae. Sci. Prog., Oxf.61, 257–274.

    Google Scholar 

  • —, 1973: The fine structure of algal cells. London: Academic Press.

    Google Scholar 

  • Drews, G., 1973: Fine structure and chemical composition of the cell envelopes. In: The biology of blue-green algae (Carr, N. G., andB. A. Whitton, eds.). Berkeley: University of California Press.

    Google Scholar 

  • Drum, R. W., andJ. T. Hopkins, 1966: Diatom locomotion: an explanation. Protoplasma62, 1–33.

    Google Scholar 

  • Dugan, P. R., C. B. MacMillan, andR. M. Pfister, 1970: Aerobic heterotrophic bacteria indigenous to pH 2.8 acid mine water: microscopic examination of acid streamers. J. Bacteriol.101, 973–981.

    PubMed  Google Scholar 

  • Dunn, J. H., andC. P. Wolk, 1970: Composition of the cellular envelopes ofAnabaena cylindrica. J. Bacteriol.103, 153–158.

    PubMed  Google Scholar 

  • Dweltz, N. E., J. R. Colvin, andA. G. McInnes, 1968: Studies on chitan [B-(1 → 4)-linked 2-acetamido-2-deoxy-D-glucan] fibers of the diatomThalassiosira fluviatilis, Hustedt. III. The structure of chitan from X-ray diffraction and electron microscope observations. Canad. J. Chem.46, 1513–1521.

    Google Scholar 

  • Friedman, B. A., andP. R. Dugan, 1968: Concentration and accumulation of metallic ions by the bacteriumZoogloea. Dev. Ind. Microbiol.9, 381–388.

    Google Scholar 

  • — —,R. M. Pfister, andC. C. Remsen, 1968: Fine structure and composition of the zoogloeal matrix surroundingZoogloea ramigera. J. Bacteriol.96, 2144–2153.

    PubMed  Google Scholar 

  • Hanke, D. E., andD. H. Northcote, 1975: Molecular visualization of pectin and DNA by ruthenium red. Biopolymers14, 1–17.

    PubMed  Google Scholar 

  • Harris, R. H., andR. Mitchell, 1973: The role of polymers in microbial aggregation. Ann. Rev. Microbiol.27, 27–50.

    Google Scholar 

  • Haug, A., B. Larsen, andE. Baardseth, 1969: Comparison of the constitution of alginates from different sources. In: Proceedings of the Sixth International Seaweed Symposium (R. Margalef, ed.). Madrid: Subsecretaria de la Marina Mercante.

    Google Scholar 

  • Ito, S., 1965: The enteric surface coat on cat intestinal microvilli. J. Cell Biol.27, 475–491.

    PubMed  Google Scholar 

  • Jirgensons, B., 1962: Natural organic macromolecules. Oxford: Pergamon Press.

    Google Scholar 

  • Jones, H. C., I. L. Roth, andW. M. Sanders, III., 1969: Electron microscopic study of a slime layer. J. Bacteriol.99, 316–325.

    PubMed  Google Scholar 

  • Jost, M., 1965: Die Ultrastruktur vonOscillatoria rubescens D. C. Arch. Mikrobiol.50, 211–245.

    Google Scholar 

  • Lagerwerff, J. V., 1960: The contact-exchange theory amended. Plant Soil13, 253–264.

    Google Scholar 

  • Lamont, H. C., 1969: Shear-oriented microfibrils in the mucilaginous investments of two motile oscillatoriacean blue-green algae. J. Bacteriol.97, 350–361.

    PubMed  Google Scholar 

  • Lang, N. J., 1968: The fine structure of blue-green algae. Ann. Rev. Microbiol.22, 15–46.

    Google Scholar 

  • Leak, L. V., 1967: Fine structure of the mucilaginous sheath ofAnabaena sp. J. Ultrastruct. Res.21, 61–74.

    PubMed  Google Scholar 

  • Lean, D. R. S., 1973 a: Phosphorus dynamics in lake water. Science (Wash.).179, 678–680.

    Google Scholar 

  • —, 1973 b: Movements of phosphorus between its biologically important forms in lake water. J. Fish. Res. Board Canad.30, 1525–1536.

    Google Scholar 

  • —, andM. N. Charlton, 1976: A study of phosphorus kinetics in a lake ecosystem. In: Environmental biogeochemistry, Volume 1. Carbon, Nitrogen, Phosphorus, Sulfur and Selenium cycles (Nriagu, J. O., ed.). Ann Arbor, Michigan: Ann Arbor Science Publishers Inc.

    Google Scholar 

  • — —, andK. R. Young, 1975: Phosphorus: changes in ecosystem metabolism from reduced loading. Verh. Internat. Verein. Limnol.19, 249–257.

    Google Scholar 

  • —, andC. Nalewajko, 1976: Phosphate exchange and organic phosphorus excretion by freshwater algae. J. Fish. Res. Board Canad.33, 1312–1323.

    Google Scholar 

  • Leppard, G. G., 1974: Rhizoplane fibrils in wheat: demonstration and derivation. Science (Wash.)185, 1066–1067.

    Google Scholar 

  • —, andJ. R. Colvin, 1971: Fibrillar lignin or fibrillar pectin? J. Polymer Sci. Part C36, 321–326.

    Google Scholar 

  • — —, 1972: Electron-opaque fibrils and granules in and between the cell walls of higher plants. J. Cell Biol.53, 695–703.

    PubMed  Google Scholar 

  • — —,D. Rose, andS. M. Martin, 1971: Lignofibrils on the external cell wall surface of cultured plant cells. J. Cell Biol.50, 63–80.

    PubMed  Google Scholar 

  • —, andS. Ramamoorthy, 1975: The aggregation of wheat rhizoplane fibrils and the accumulation of soil-bound cations. Canad. J. Bot.53, 1729–1735.

    Google Scholar 

  • Luft, J. H., 1971: Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat. Rec.171, 347–368.

    PubMed  Google Scholar 

  • Martinez-Palomo, A., 1970: The surface coats of animal cells. Int. Rev. Cytol.29, 29–75.

    Google Scholar 

  • Nevins, D. J., P. D. English, andP. Albersheim, 1967: The specific nature of plant cell wall polysaccharides. Plant Physiol.42, 900–906.

    Google Scholar 

  • Nichols, H. W., andH. C. Bold, 1965:Trichosarcina polymorpha gen. et sp. nov. J. Phycol.1, 34–38.

    Google Scholar 

  • O'Colla, P. S., 1962: Mucilages. In: Physiology and biochemistry of algae (Lewin, R. A., ed.). New York: Academic Press.

    Google Scholar 

  • Paerl, H. W., andD. R. S. Lean, 1976: Visual observations of phosphorus movement between algae, bacteria, and abiotic particles in lake waters. J. Fish. Res. Board Canad.33, 2805–2813.

    Google Scholar 

  • —, andS. L. Shimp, 1973: Preparation of filtered plankton and detritus for study with scanning electron microscopy. Limnol. Oceanogr.18, 802–805.

    Google Scholar 

  • Pate, J. L., andE. J. Ordal, 1967: The fine structure ofChondrococcus columnaris. III. The surface layers ofChondrococcus columnaris. J. Cell Biol.35, 37–51.

    PubMed  Google Scholar 

  • Pennington, W., 1974: Seston and sediment formation in five Lake District lakes. J. Ecol.62, 215–251.

    Google Scholar 

  • Pickett-Heaps, J. D., 1975: Green algae-structure, reproduction and evolution in selected genera. Sunderland, Mass.: Sinauer Associates.

    Google Scholar 

  • Ramamoorthy, S., and G. G.Leppard, 1977 a: Fibrillar pectin and contact cation exchange at the root surface. J. theor. Biol. In press.

  • - - 1977 b: Root surfaces and accretion of lead. Part two. A structural analysis of the mechanism. J. Inorg. Nucl. Chem. In press.

  • Remsen, C. C., andS. W. Watson, 1972: Freeze-etching of bacteria. Int. Rev. Cytol.33, 253–296.

    PubMed  Google Scholar 

  • Reynolds, E. S., 1963: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol.17, 208–212.

    PubMed  Google Scholar 

  • Rorem, E. S., 1955: Uptake of rubidium and phosphate ions by polysaccharide-producing bacteria. J. Bacteriol.70, 691–701.

    PubMed  Google Scholar 

  • Salton, M. R. J., 1964: The bacterial cell wall. Amsterdam: Elsevier Publishing Co.

    Google Scholar 

  • Spurr, A. R., 1969: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res.26, 31–43.

    PubMed  Google Scholar 

  • Staehelin, L. A., andJ. D. Pickett-Heaps, 1975: The ultrastructure ofScenedesmus (Chlorophyceae). I. Species with the “reticulate” or “warty” type of ornamental layer. J. Phycol.11, 163–185.

    Google Scholar 

  • Starr, R. C., 1964: The culture collection of algae at Indiana University. Amer. J. Bot.51, 1013–1044.

    Google Scholar 

  • Sterling, C., 1970: Crystal-structure of ruthenium red and stereochemistry of its pectin stain. Amer. J. Bot.57, 172–175.

    Google Scholar 

  • Wang, W. S., andR. G. Tischer, 1973: Study of the extracellular polysaccharides produced by a blue-green alga,Anabaena flos-aquae A-37. Arch. Mikrobiol.91, 77–81.

    PubMed  Google Scholar 

  • Wetzel, R. G., 1975: Limnology. Philadelphia: W. B. Saunders Co.

    Google Scholar 

  • Whistler, R. L., 1973: Industrial gums — polysaccharides and their derivatives. Second edition. New York: Academic Press.

    Google Scholar 

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Leppard, G.G., Massalski, A. & Lean, D.R.S. Electron-opaque microscopic fibrils in lakes: Their demonstration, their biological derivation and their potential significance in the redistribution of cations. Protoplasma 92, 289–309 (1977). https://doi.org/10.1007/BF01279466

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