Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-29T01:47:19.593Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of a humic acid extracted from marine sediment and its influence on the growth of marine diatoms

Published online by Cambridge University Press:  08 April 2014

Marcela V. Martin ,
Christina Gebühr ,
Daniel O. Mártire  and
Karen H. Wiltshire
Marcela V. Martin*
Affiliation:
Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas (INIFTA, CONICET/UNLP), Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina
Christina Gebühr
Affiliation:
Institute of Geosciences, Goethe-University Frankfurt, 60438 Frankfurt am Main, Germany and Biodiversity and Climate Research Center (BIK-F), 60325 Frankfurt am Main, Germany
Daniel O. Mártire
Affiliation:
Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas (INIFTA, CONICET/UNLP), Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina
Karen H. Wiltshire
Affiliation:
Biologische Anstalt Helgoland, Alfred Wegener Institute for Polar and Marine Research, POB 180, 27489 Helgoland, Germany
*
Correspondence should be addressed to: M.V. Martin, Casilla de correo 16, sucursal 4 (1900), La Plata, Argentina email: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Due to the input of humic substances from freshwater run-off into the marine habitat, the influences of such substances on marine organisms should not be neglected. We here investigate the effect of a humic acid (HA) extract from the North Sea, characterized by spectroscopic techniques and carboxylic and phenolic group content, on the growth of different algae. Two benthic pennate diatoms isolated from the Baltic Sea, Navicula ramosissima (C. Agardh) Cleve, 1895 and Entomoneis paludosa (W. Smith) Reimer, 1975, as well as two tychopelagic centric diatoms isolated from the North Sea, Melosira nummuloides C. Agardh, 1824 and Paralia sulcata (Ehrenberg) Cleve, 1873, were employed. The concentrations of pigments (fucoxanthin, diadinoxanthin, chlorophyll-a and β-carotene) and nutrients were also measured. Adding low concentrations of naturally humic substances (5.5 mg of C l−1) to the algae cultures resulted in enhanced growth rates compared to the control experiments, possibly due to the increase in the bioavailability of trace metals or other nutrients.

Keywords

Helgoland Roadshumic substancesmarine diatomsNorth SeaParalia sulcatagrowth experiments
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 5 , August 2014 , pp. 895 - 906
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aiken, G.R., McKnight, D.M., Wershaw, R.L. and MacCarthy, P. (1985) An introduction to humic substances in soils, sediments and waters. In Aiken, G.R., McKnight, D.M., Wershaw, R.L. and MacCarthy, P. (eds) Humic substances in soil, sediment and water. New York: John Wiley & Sons, pp. 1–9.Google Scholar
Amir, S., Hafidi, M., Bailly, J-R. and Revel, J-C. (2003) Characterization of humic acids extracted from sewage sludge during composting and of their Sephadex® gel fractions. Agronomie 23, 269–275.Google Scholar
Andjelkovic, T., Perovic, J., Purenovic, M., Бlagojevic, S., Nikolic, R., Andjelkovic, D. and Bojic, A. (2006) Spectroscopic and potentiometric studies on derivatized natural humic acid. Analytical Sciences 22, 1553–1558.Google Scholar
Bährs, H. and Steinberg, C.E.W. (2012) Impact of two different humic substances on selected coccal green algae and Cyanobacteria-changes in growth and photosynthetic performance. Environmental Science and Pollution Research 19, 335–346.CrossRefGoogle ScholarPubMed
Beck, M., Olaf, Dellwig O., Fischer, S., Schnetger, B. and Brumsack, H.-J. (2012) Trace metal geochemistry of organic carbon-rich watercourses draining the NW German coast. Estuarine, Coastal and Shelf Science 104/105, 66–79.Google Scholar
Beutler, M., Wiltshire, K.H., Meyer, B., Moldaenke, C., Luring, C., Meyerhofer, M., Hansen, U. P. and Dau, H. (2002) A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynthesis Research 72, 39–53.CrossRefGoogle ScholarPubMed
Bosio, G.N., David Gara, P., García Einschlag, F.S., Gonzalez, M.C., del Panno, M.T. and Mártire, D.O. (2008) Photodegradation of soil organic matter and its effect on gram (-) bacterial growth. Photochemistry & Photobiology 84, 1126–1132.CrossRefGoogle ScholarPubMed
Campbell, P.G.C. (1995) Interactions between trace metals and aquatic organisms: A critique of the free-ion activity model. In Tessier, A. and Turner, D.R. (eds) Metal speciation and bioavailability in aquatic systems. New York: John Wiley & Sons, pp. 45–102.Google Scholar
Carder, K.L., Steward, R.G., Harvey, G.R. and Ortner, P.B. (1989) Marine humic and fulvic acids: their effects on remote sensing of ocean chlrophyll. Limnology and Oceanography 34, 68–81.Google Scholar
Carlos, L., Pedersen, B.W., Ogilby, P.R. and Mártire, D.O. (2011) The role of humic acid aggregation on the kinetics of photosensitized singlet oxygen production and decay. Photochemical and Photobiological Science 10, 1080–1086.Google Scholar
Chen, J., Gu, B., Leboeuf, B.J., Pan, H. and Dai, S. (2002) Spectroscopic characterization of the structural and functional properties of natural organic matter fractions. Chemosphere 48, 59–68.Google Scholar
Chen, M. and Wang, W-X. (2008) Accelerated uptake by phytoplankton of iron bound to humic acids. Aquatic Biology 3, 155–166.Google Scholar
Chen, W., Westerhoff, P., Leenheer, J.A. and Booksh, K. (2003) Fluorescence excitation–emission matrix regional integration to quantify spectra for dissolved organic matter. Environmental Science and Technology 37, 5701–5710.Google Scholar
Chen, Y., Senesi, N. and Schnitzer, M. (1977) Information provided on humic substances by E4–E6 ratios. Soil Science Society of America Journal 41, 352–358.Google Scholar
Chen, Z., Porcher, C., Campbell, P.G.C. and Fortin, C. (2013) Influence of humic acid on algal uptake and toxicity of ionic silver. Environmental Science and Technology 47, 8835–8842.Google Scholar
Chin, Y.P., Aiken, G. and O'Loughlin, E. (1994) Molecular weight, polydispersity and spectroscopic properties of aquatic humic substances. Environmental Science and Technology 28, 1853–1858.CrossRefGoogle ScholarPubMed
Coble, P.G. (1996) Characterization of marine and terrestrial DOM in seawater using excitation–emission matrix spectroscopy. Marine Chemistry 51, 325–346.Google Scholar
Daehnick, A.E., Sullivan, M.J. and Moncreiff, C.A. (1992) Primary production of the sand microflora in seagrass beds of Mississippi Sound. Botanica Marina 35, 131–139.Google Scholar
Del Vecchio, R. and Blough, N.V. (2002) Photobleaching of chromophoric dissolved organic matter in natural waters: kinetics and modeling. Marine Chemistry 78, 231–253.Google Scholar
Franke, H-D., Bucholz, F. and Wiltshire, K.H. (2004) Ecological long-term research at Helgoland (German Bight, North Sea): retrospect and prospect—an introduction. Helgoland Marine Research 58, 223–229.Google Scholar
Frost, B.W. (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 14, 805–815.CrossRefGoogle Scholar
Ghabbour, E.A. and Davies, G. (2005) Humic substances: molecular details and applications in land and water conservation. New York: Taylor & Francis.Google Scholar
Graham, L.E. and Wilcox, L.W. (2000). Ochrophytes. Part 2. Diatoms. In Algae. Upper Saddle River, NJ: Prentice-Hall, Chapter 12.Google Scholar
Grasshoff, K. (1976) Methods of seawater analysis. Weinheim: Verlag Chemie.Google Scholar
Guillard, R.R.L. and Ryther, J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Canadian Journal of Microbiology 8, 229–239.Google Scholar
Hellebost, J.A. and Guillaro, R.R.L. (1967) Uptake specificity for organic substrates by the marine diatom Melosira nummuloides. Journal of Phycology 3, 132–136.Google Scholar
Hillebrand, H., Dürselen, C.D., Kirschtel, D., Pollingher, U. and Zohary, T. (1999) Biovolume calculating for pelagic and benthic microalgae. Journal of Phycology 35, 403–424.Google Scholar
Imai, A., Fukushima, T. and Matsushige, K. (1999) Effects of iron limitation and aquatic humic substances on the growth of Microcystis aeruginosa. Canadian Jourmal of Fisheries and Aquatic Science 56, 1929–1937.Google Scholar
IHSS (Internacional Humic Substances Society) (2008) Available at: http://www.humicsubstances.org/Google Scholar
Knefelkamp, B., Carstens, K. and Wiltshire, K.H. (2007) Comparison of different filter types on chlorophyll-a retention and nutrient measurements. Journal of Experimental Marine Biology and Ecology 345, 61–70.CrossRefGoogle Scholar
Lguirati, A., Ait Baddi, G., El Mousadik, A., Gilard, V., Revel, J.C. and Hafidi, M. (2005) Analysis of humic acids from aerated and non-aerated urban landfill composts. International Biodeterioration & Biodegradation 56, 8–16.Google Scholar
Lund, W. (1990) The complexation of metal ions by humic substances in natural waters. In Broekaert, JAC, Güçer, S. and Adams, F. (eds) Metal speciation in the environment. Berlin: Springer-Verlag, pp. 43–56.Google Scholar
MacIntyre, H.L., Geider, R.J. and Miller, D.C. (1996) Microphytobenthos: the ecological role of the ‘secret garden’ of unvegetated, shallow-water marine habitats. 1. Distribution, abundance and primary production. Estuaries 19, 186–201.Google Scholar
McLean, R.O., Corrigan, J. and Webster, J. (1981) Heterotrophic nutrition in Melosira nummuloides, a possible role in affecting distribution in the Clyde Estuary. European Journal of Phycology 16, 95–106.Google Scholar
McQuoid, M.R. and Hobson, L.A. (1998) Assessment of palaeoenvironmental conditions on Southern Vancouver Island, British Columbia, Canada, using the marine tychopankter Paralia sulcata. Diatom Research 13, 311–321.Google Scholar
McQuoid, M.R. and Nordberg, K. (2003) The diatom Paralia sulcata as an environmental indicator species in coastal sediments. Estuarine, Coastal and Shelf Science 56, 339–354.CrossRefGoogle Scholar
Mignone, R.A., Martin, M.V., Morán Vieyra, F.E., Palazzi, V.I., López de Mishima, B., Mártire, D.O. and Borsarelli, C.D. (2012) Modulation of optical properties of dissolved humic substances by their origin and molecular complexity. Photochemistry and Photobiology 88, 792–800. [Special Issue on the 21st Conference of the IAPS.]Google Scholar
Moreda-Piñeiro, A., Bermejo-Barrera, A. and Bermejo-Barrera, P. (2004) New trends involving the use of ultrasound energy for the extraction of humic substances from marine sediments. Analytica Chimica Acta 524, 97–107.Google Scholar
Moreda-Piñeiro, A., Seco-Gesto, E.M., Bermejo-Barrera, A. and Bermejo-Barrera, P. (2006) Characterization of surface marine sediments from Ría de Arousa estuary according to extractable humic matter content. Chemosphere 64, 866–873.CrossRefGoogle ScholarPubMed
Nardi, S., Pizzeghello, D., Muscolo, A. and Vianello, A. (2002) Physiological effects of humic substances on higher plants. Soil Biology & Biochemistry 34, 1527–1536.Google Scholar
Parlanti, E., Morin, B. and Vache, L. (2002) Combined 3D-spectrofluorometry, high performance liquid chromatography and capillary electrophoresis for the characterization of dissolved organic matter in natural waters. Organic Geochemistry 33, 221–223.Google Scholar
Pinckney, J.L. and Zingmark, R.G. (1993) Modelling the annual production of intertidal benthic microalgae in estuarine ecosystems. Journal of Phycology 29, 396–407.Google Scholar
Prakash, A. and Rashid, M.A. (1968) Influence of humic substances on the growth of marine phytoplankton: dinoflagellates. Limnology and Oceanography 13, 598–606.Google Scholar
Prakash, A., Rashid, M.A., Jensen, A. and Subbarao, D.V. (1973) Influence of humic substances on growth of marine phytoplankton–diatoms. Limnology and Oceanography 18, 516–524.Google Scholar
Prokhotskaya, V.Y. and Steinberg, C.E.W. (2007) Differential sensitivity of a coccal green algae and a cyanobacterial species to dissolved natural organic matter (NOM). Environmental Science and Pollution Research 14, 11–18.Google Scholar
Rashid, M.A. (1971) Role of humic acids of marine origin and their different molecular weight fractions in complexing di- and trivalent metals. Soil Science 111, 298–306.Google Scholar
Roelofs, A.K. (1984) Distributional patterns and variation of valve diameter of Paralia sulcata in surface sediments of Southern British Columbia Inlets. Estuarine, Coastal and Shelf Science 18, 165–176.Google Scholar
Sánchez-Marín, P. and Beiras, R. (2011) Adsorption of different types of dissolved organic matter to marine phytoplankton and implications for phytoplankton growth and Pb bioavailability. Journal of Plankton Research 33, 1396–1409.CrossRefGoogle Scholar
Steinberg, C.E.W., Kamara, S., Prokhotskaya, V.Y., Manusadzianas, L., Karasyova, T.A., Timofeyev, M.A., Jie, Z., Paul, A., Meinelt, T., Farjalla, V.F., Matsuo, A.Y.O., Burnison, B.K. and Menzel, R. (2006) Dissolved humic substances: Ecological driving forces from the individual to the ecosystem level? Freshwater Biology 51, 1189–1210.Google Scholar
Schnitzer, M. and Khan, S.U. (1972) Humic subtances in the enviroment. New York: Marcel Dekker.Google Scholar
Schnitzer, M. and Gupta, U.C. (1965) Determination of acidity in soil organic matter. Soil Science Society of America Proceedings 29, 274–277.Google Scholar
Sierra, M.M.D., Donard, O.F.X. and Lamotte, M. (1997) Behaviour of dissolved fluorescent organic matter during estuarine mixing. Marine Chemistry 58, 51–58.CrossRefGoogle Scholar
Sierra, M.M.D., Donard, O.F.X., Lamotte, M., Belin, C. and Ewald, M. (1994) Fluorescence spectroscopy of coastal and marine waters. Marine Chemistry 47, 127–144.Google Scholar
Sierra, M.M.D., Giovanela, M., Parlanti, E. and Soriano-Sierra, E.J. (2005) Fluorescence fingerprint of fulvic and humic acids from varied origins as viewed by single-scan and excitation/emission matrix techniques. Chemopshere 58, 715–733.Google Scholar
Silva, M.R. (1996) Estudos potenciométricos e fluorimétricos dos equilíbrios ácido-básicos e da complexação de metáis com o Obisdien e as substãncias húmicas. Contaminação pelos metais em sedimentos da Ilha de Santa Catarina (Brasil). PhD thesis. Universidad e Federal de Santa Catarina, Brazil.Google Scholar
Song, Z., Chouparova, E., Jones, K.W., Feng, H. and Marinkovic, N.S. (2001) FTIR investigation of sediments from NY/NJ Harbor, San Diego Bay and the Venetian Lagoon. NSLS Activity Report, Z-112-Z-116.Google Scholar
Steinberg, C.E.W., Kamara, S., Prokhotskaya, V.Y., Manusadzianas, L., Karasyova, T.A., Timofeyev, M.A., Jie, Z., Paul, A., Meinelt, T., Farjalla, V.F., Matsuo, A.Y.O, Burnison, B.K. and Menzel, R. (2006) Dissolved humic substances. Ecological driving forces from the individual to the ecosystem level? Freshwater Biology 51, 1189–1210.Google Scholar
Wilkinson, M., Henderson, A.R. and Wilkinson, C. (1976) Distribution of attached algae in estuaries. Marine Pollution Bulletin 7, 183.Google Scholar
Wiltshire, K.H. (2000) Algae and associated pigments of intertidal sediments; new observations and methods. Limnologica 30, 205–214.Google Scholar
Wiltshire, K.H., Harsdorf, S., Smidt, B., Blocker, G., Reuter, R. and Schroeder, F. (1998) The determination of algal biomass (as chlorophyll) in suspended matter from the Elbe estuary and the German Bight: a comparison of high-performance liquid chromatography, delayed fluorescence and prompt fluorescence methods. Journal of Experimental Marine Biology and Ecology 222, 113–131.CrossRefGoogle Scholar
Wiltshire, K.H. and Manly, B.F.J. (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgoland Marine Research 58, 269–273.Google Scholar
Wolff, W.J. (1979) Flora and vegetation of the Wadden Sea. Report 3. In Final Report of the Section Marine Biology of the Wadden Sea. Rotterdam: A.A. Balkema.Google Scholar
Zhang, Y., Du, J., Zhang, F., Yu, Y. and Zhang, J. (2011) Chemical characterization of humic substances isolated from mangrove swamp sediments: the Qinglan area of Hainan Island, China. Estuarine, Coastal and Shelf Science 92, 180–187.Google Scholar
Zong, Y. (1997) Implications of Paralia sulcata abundance in Scottish isolation basins. Diatom Research 12, 125–150.Google Scholar