Possible Fe Isotope Fractionation During Microbiological Processing in Ancient and Modern Marine Environments

  • Alain R. PréatEmail author
  • Jeroen T. M. De Jong
  • Chantal De Ridder
  • David C. Gillan
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 18)


Eight iron (Fe) isotopic compositions of iron deposits in biofilms and granules found in two recent burrowing marine invertebrates (the sea urchin ­Echinocardium cordatum and the bivalve Montacuta ferruginosa) were obtained by Multiple-Collector Inductively Coupled Plasma Mass Spectrometry (MC-ICP-MS). δ56Fe values ranged between –1.78‰ and −0.74‰. The lightest δ56Fe is ­associated with the iron granules in the intestinal wall of E. cordatum and may be due to the abiotic oxidation of source Fe(II) with an isotopic composition reflecting that of light reduced Fe in sediment porewater. This lightest value could represent the best value for the pristine value. Fe in the biofilms was typically heavier by up to +1‰, mean ∼ +0.7‰. These results are compared with Fe isotopic composition of 17 Jurassic limestones from the Rosso Ammonitico Veronese (Italy) containing red and gray hemipelagic facies. The red facies show clear evidence of iron bacteria and fungi, which are interpreted as a possible equivalent of the iron microbial communities associated with the recent organisms. Pronounced Fe isotope fractionation was observed in the Jurassic red hardground levels and in the more condensed red facies where bacteria and fungi lived and have accumulated, with values ­typically lighter by −1‰ than the gray facies where microorganisms were absent. This fractio­nation probably involved the passive accumulation of originally light porewater Fe in the exopolymeric substances (EPS) produced by filamentous bacteria, thereby favoring heavier Fe isotopes. Alternating stages of oxidation Fe(II)/Fe(III) occurred near the sediment/water interfaces as a consequence of microenvironmental changes in the marine porewaters and caused the red/gray facies interlayering. The comparison of the Fe isotopic compositions of the “biominerals” in the recent organisms and in the iron minerals of the red and gray Jurassic facies suggests an isotopic biofractionation of at least ∼+0.7‰. Both studied organisms (the sea urchin and the bivalve) thrive in similar microenvironmental conditions as the ­microorganisms of the condensed red facies. Their Fe isotope compositions are the same, as is the range of the probable biofractionation.


Iron isotopes Microbial mediation Italian Jurassic Rosso Ammonitico Recent sea urchins and bivalves 



This study was financially supported by the Belgian Fonds National de la Recherche Scientifique (FNRS) (FRFC grant no. 2.4.578.08F) to A. Préat and FRFC grant no. 2.4594.07 to C. De Ridder. The FNRS also supported the development of the MC-ICP-MS facility at the ULB, and we are thankful to N. Mattielli and C. Maerschalk for maintaining the facility and its associated labs in excellent shape. F. Poitrasson and J. Wiederhold are thanked for providing the ETH in-house standards. This is a contribution of the Centre Interuniversitaire de Biologie Marine (CIBIM). Comments by L. Martire (U. of Torino, Italy) are gratefully acknowledged.


  1. Abraham, K., Opfergelt, S., Fripiat, F., Cavagna, A.-J., de Jong, J.T.M., Foley, S., André, L. and Cardinal, D. (2008) δ30Si and δ29Si determinations on USGS BHVO-1 and BHVO-2 reference materials with a new configuration on a Nu Plasma multi-collector ICP-MS. Geostand. Geoanal. Res. 32: 193–202.CrossRefGoogle Scholar
  2. Balci, N., Bullen, T.D., Witte-Lien, K., Shanks, W.C., Motleica, M. and Mandernack, K.W. (2006) Iron isotope fractionation during microbially stimulated Fe(II) oxidation and Fe(III) precipitation. Geochim. Cosmochim. Acta 70: 622–639.CrossRefGoogle Scholar
  3. Beard, B.L., Johnson, C.M., Skulan, J.L., Nealson, K.H., Cox, L. and Sun, H. (2003a) Application of Fe isotopes to tracing the geochemical and biological cycling of Fe. Chem. Geol. 195: 87–117.CrossRefGoogle Scholar
  4. Beard, B.L., Johnson, C.M., Von Damm, K.L. and Poulson, R.L. (2003b) Iron isotope constraints on Fe cycling and mass balance in oxygenated Earth oceans. Geology 31: 629–632.CrossRefGoogle Scholar
  5. Beard, B.L. and Johnson, C.M. (2004). Fe isotopes variations in the Modern and Ancient earth and other planetory bodies. In Geochemistry of non-traditional stable isotopes, Reviews in Mineralogy and Geochemistry, Mineralogical Society of America 55: 319–357.CrossRefGoogle Scholar
  6. Bensing, J.P., Mozley, P.S. and Dunbar, N.W. (2005) Importance of clay in iron transport and sediment reddening: evidence from reduction features of the Abo Formation, New Mexico, U.S.A. J. Sediment Res. 75: 562–571.CrossRefGoogle Scholar
  7. Boulvain, F., De Ridder Ch., Mamet, B., Préat, A. and Gillan, D. (2001) Iron microbial communities in Belgian Frasnian carbonate mounds. Facies 44: 47–60.CrossRefGoogle Scholar
  8. Brantley, S.L., Liermann, L.J. and Bullen, T. (2001) Fractionation of Fe isotopes by soil microbes and organic acids. Geology 29: 535–538.CrossRefGoogle Scholar
  9. Brantley, S.L., Liermann, L.J., Guynn, R.L., Anban, A., Icopini, G.A. and Barling, J. (2004) Fe isotopic fracionation during mineral dissolution with and without bacteria. Geochim. Cosmochim. Acta 68: 3189–3204.CrossRefGoogle Scholar
  10. Buchanan, J.B., Brown, B.E., Coombs, T.E., Pirie, B.J.S. and Allen, J.A. (1980) The accumulation of ferric iron in the guts of some spatangoid echinoderms. J. Mar. Biol. Assoc. UK 60: 631–640.CrossRefGoogle Scholar
  11. Byrne, R.H. and Kester, D.R. (1976) Solubility of hydrous ferric oxide and iron speciation in seawater. Mar. Chem. 4: 255–274.Google Scholar
  12. Canfield, D.E., Thamdrup, B. and Hansen, J.W. (1993) The anaerobic degradation of organic matter in Danish coastal sediments: Iotn reduction, manganese reduction, and sulfate reduction. Geochim. Cosmochim. Acta 57: 3867–3883.PubMedCrossRefGoogle Scholar
  13. Clari, P.A. and Martire, L. (1996) Interplay of cementation, mechanical compaction, and chemical compaction in nodular limestones of the Rosso Ammonitico Veronese (Middle-Upper Jurassic, Northeastern Italy). J. Sediment Res. 66: 447–458.Google Scholar
  14. Clari, P.A., Marini, P., Pastorini, M. and Pavia, G. (1984) Il Rosso Ammonitico Inferiore (Bajociano-Calloviano) nei Monti Lessini settentrionali. Riv. It. Paleont Strat. 90: 15–86.Google Scholar
  15. Crosby, H.A., Johnson, C.M., Roden, E.E. and Beard, B.L. (2005) Coupled Fe(II)-Fe(III) electron and atom exchange as a mechanism for Fe isotope fractionation during dissimilatory iron oxide reduction. Environ. Sci. Technol. 39: 6698–6704.PubMedCrossRefGoogle Scholar
  16. Gomes da Silva, S., Gillan, D., Dubilier, N. and De Ridder, C. (2006) Characterization by 16S rRNA gene analysis and in situ hybridization of bacteria living in the hindgut of a deposit-feeding echinoid (Echinodermata). J. Mar. Biol. Assoc. U.K. 86: 1209–1213.Google Scholar
  17. de Jong, J.T.M., Schoemann, V., Tison, J.-L., Becquevort, S., Masson, F., Lannuzel, D., Petit, J., Chou, L., Weis, D. and Mattielli, N. (2007) Precise measurement of iron isotopes in marine samples by multi-collector inductively coupled plasma mass spectrometry. Anal. Chim. Acta 589: 105–119.PubMedCrossRefGoogle Scholar
  18. de Jong, J., Schoemann, V., Lannuzel, D., Tison, J.-L. and Mattielli, N. (2008) High-accuracy determination of iron in seawater by isotope dilution multiple collector inductively coupled plasma mass spectrometry (ID-MC-ICP-MS) using nitrilotriacetic acid chelating resin for preconcentration and matrix separation. Anal. Chim. Acta 623: 126–139.PubMedCrossRefGoogle Scholar
  19. De Ridder, C. (1994) Symbioses between spatangoids (Echinoidea) and Thiothrix-like bacteria (Beggiatoales), In: B. David, A. Guille, J.P. Feral and M. Roux (eds.) Echinoderms Through Time; Proceedings of 8th International Echinoderm Conference, Dijon 1993. Balkema, Rotterdam, pp. 619–625.Google Scholar
  20. De Ridder, C. and Brigmon, R.L. (2003) “Farming” of microbial mats in the hindgut of echinoids, In: W.E. Krumbein, D.M. Paterson and G.A. Zavarzin (eds.) Fossil and Recent Biofilms: A Natural History of Life on Earth. Kluwer Academic, Boston, pp. 217–225.Google Scholar
  21. De Ridder, C. and Jangoux, M. (1993) The digestive tract of the spatangoid echinoid Echinocardium cordatum (Echinodermata): morphofunctional study. Acta Zool. 74: 337–351.CrossRefGoogle Scholar
  22. De Ridder, C., Jangoux, M. and De Vos, L. (1985) Description and significance of a peculiar intradigestive symbiosis between bacteria and a deposit-feeding echinoid. J. Exp. Mar. Biol. Ecol. 91: 65–76.CrossRefGoogle Scholar
  23. Dideriksen, K., Baker, J.A. and Stipp, S.L.S. (2006) Iron isotopes in natural carbonate minerals determined by MC-ICP-MS with a 58Fe–54Fe double spike. Geochim. Cosmochim. Acta 70: 118–132.CrossRefGoogle Scholar
  24. Emerson, D. and Moyer, C. (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl. Environ. Microbiol. 63: 4784–4792.PubMedGoogle Scholar
  25. Fantle, M.S. and DePaolo, D.J. (2004) Iron isotopic fractionation during continental weathering. Earth Planet. Sci. Lett. 228: 547–562.CrossRefGoogle Scholar
  26. Fehr, M.A., Andersson, P.S., Hålenius, U. and Mörth, C.-M. (2008) Iron isotope variations in Holocene sediments of the Gotland Deep, Baltic Sea. Geochim. Cosmochim. Acta 72: 807–826.CrossRefGoogle Scholar
  27. Fenchel, T. and Finlay, J. (1995) Ecology and Evolution in Anoxic Worlds. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford, pp. 276.Google Scholar
  28. Fortin, D. and Langley, S. (2005) Formation and occurrence of biogenic iron-rich minerals. Earth Sci. Rev. 72: 1–19.CrossRefGoogle Scholar
  29. Gage, J. (1966) Observations on the bivalves Montacuta substriata and M. ferruginosa, “commensals” with spatangoids. J. Mar. Biol. Assoc. UK 46: 49–70.CrossRefGoogle Scholar
  30. Gillan, D. (2003) The study of a Recent iron-encrusted biofilm in the marine environment, In: W.E. Krumbein, D.M. Paterson and G.A. Zavarzin (eds.) Fossil and Recent Biofilms: A Natural History of Life on Earth. Kluwer Academic, Boston, pp. 241–248.Google Scholar
  31. Gillan, D. and De Ridder, C. (1995) The microbial community associated with Montacuta ferruginosa, a commensal bivalve of the echnoid Echinocardium cordatum, In: R.H. Emson, A.B. Smith and A.C. Campbell (eds.) Proceedings of 4th European Echinoderm Conference, London. Balkema, Rotterdam, pp. 71–76.Google Scholar
  32. Gillan, D. and De Ridder, C. (1997) Morphology of ferric iron-encrsuted biofilm forming on the shell of a burrowing bivalve (Mollusca). Aquat. Microb. Ecol. 12: 1–10.CrossRefGoogle Scholar
  33. Gillan, D.C. and De Ridder, C. (2001) Accumulation of a ferric mineral in the biofilm of Montacuta ferruginosa (Mollusca, Bivalvia). Biomineralization, bioaccumulation, and inference of paleoenvironments, Chem. Geol. 177: 371–379.CrossRefGoogle Scholar
  34. Gillan, D.C., Speksnijder, A.G.C.L., Zwart, G. and De Ridder, C. (1998) Genetic diversity of the biofilm covering Montacuta ferruginosa (Mollusca, Bivalvia) as evaluated by denaturing gradient gel electrophoresis analysis and cloning of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 64: 3464–3472.Google Scholar
  35. Gillan, D.C., Warnau, M., De Vrind-de-Jong, E.W., Boulvain, F., Préat, A. and De Ridder, C. (2000) Iron oxidation and deposition in the biofilm covering Montacuta ferruginosa (Mollusca, Bivalvia). Geomicrobiol. J. 17: 147–151.Google Scholar
  36. Hallberg, R. and Ferris, F.G. (2004) Biomineralization by Gallionella. Geomicrobiol. J. 21: 325–330.CrossRefGoogle Scholar
  37. Hofstetter, T.B., Schwarzenbach, R.P and Haderlein, S.B. (2003) Reactivity of Fe(II) species associated with clay minerals. Environ. Sci. Technol. 37: 519–528.PubMedCrossRefGoogle Scholar
  38. Icopini, G.A., Anbar, A.D., Ruebush, S.S., Tien, M. and Brantley, S.L. (2004) Iron isotope fractionation during microbial reduction of iron: the importance of adsorption. Geology 32: 205–208.CrossRefGoogle Scholar
  39. Jenkyns, H.C. (1974) Origin of red nodular limestones (Ammonitico Rosso, Knollenkalke) in the Mediterranean Jurassic: a diagenetic model, In: K.J. Hsü and H.C. Jenkyns (eds.) Pelagic Sediments: On Land and Under Sea 1. International Association Sedimentologists Special Publication, pp. 249–271.Google Scholar
  40. Johnson, C.M., Beard, B.L., Roden, E.E., Newman, D.K. and Nealson, K.H. (2004) Isotopic constraints on biogeochemical cycling of Fe. Rev. Min. Geochem. 55: 359–408.CrossRefGoogle Scholar
  41. Johnson, C.M., Beard, B.L. and Roden, E.E. (2008) The iron isotope fingerprints of redox and biogeochemical cycling in Modern and Ancient Earth. Annu. Rev. Earth Planet. Sci. 36: 457–493.CrossRefGoogle Scholar
  42. Krynine, P.D. (1949) The origin of red beds. N.Y. Acad. Sci. Trans. Ser. II 2: 60–68.CrossRefGoogle Scholar
  43. Krynine, P.D. (1950) Petrology, stratigraphy, and origin of the Triassic sedimentary rocks of Connecticut. CT. Geol. Surv. Bull. 73: 273.Google Scholar
  44. Libes, S.M. (1992) An introduction to marine biogeochemistry. Wiley, New York, 734 pp.Google Scholar
  45. Little, B.J., Wagner, P.A. and Lewandowski, Z. (1997) Spatial relationships between bacteria and mineral surfaces, In: J.F. Banfield and K.H. Nealson (eds.) Interaction Between Microbes and Minerals. Rev. Min. 35: 123–159.Google Scholar
  46. Loreau, J.P. (1972) Pétrographie des calcaires fins au microscope électronique à balayage: introduction à une classification des micrites. C.R. Acad. Sci. Paris 274: 810–813.Google Scholar
  47. Mamet, B. and Préat, A. (2003) Sur l’origine de la pigmentation de l’Ammonitico Rosso (Jurassique, région de Vérone, Italie du Nord). Rev. Micropal. 46: 35–46.CrossRefGoogle Scholar
  48. Mamet, B. and Préat, A. (2006) Iron-bacterial mediation in Phanerozoic red limestones: state of the art. Sediment. Geol. 185: 147–157.CrossRefGoogle Scholar
  49. Maréchal, C., Télouk, P. and Albarède, F. (1999) Precise analysis of copper and zinc isotopic compositions by plasma source mass spectrometry. Chem. Geol. 156: 251–273.CrossRefGoogle Scholar
  50. Martire, L. (1996) Stratigraphy, facies and synsedimentary tectonics in the Jurassic Rosso Ammonitico Veronese (Altopiano di Asiago, NE Italy). Facies 35: 209–236.CrossRefGoogle Scholar
  51. Massari, F. (1981) Cryptalgal fabrics in the Rosso Ammonitico sequences of Venetian Alps, In: A. Farinaci and S. Elmi (eds.) Rosso Ammonitico Symposium Proceedings. Tecnoscienza, Roma, pp. 435–469.Google Scholar
  52. Miller, D.N. and Folk, R.L. (1955) Occurrence of detrital magnetite and ilmenite in red sediments: new approach to significance of redbeds. Am. Assoc. Petrol. Geol. Bull. 39: 338–395.Google Scholar
  53. Munn, C.B. (2004) Marine Microbiology: Ecology and Application. Garland, London, 282p.Google Scholar
  54. Poitrasson, F. and Freydier, R. (2005) Heavy iron isotope composition of granites determined by high resolution MC-ICP-MS. Chem. Geol. 222: 132–147.CrossRefGoogle Scholar
  55. Préat, A., Mamet, B., Bernard, A. and Gillan, D. (1999) Bacterial mediation, red matrices diagenesis, Devonian, Montagne Noire (southern France). Sediment. Geol. 126: 223–242.CrossRefGoogle Scholar
  56. Préat, A., Morano, S., Loreau, J.P., Durlet, C. and Mamet, B. (2006) Petrography and biosedimentology of the Rosso Ammonitico Veronese (Middle-Upper Jurassic, Northeastern Italy). Facies 52: 265–278.CrossRefGoogle Scholar
  57. Préat, A., de Jong, J., Mamet, B. and Mattielli, N. (2008a) Stable isotope and microbial mediation in red pigmentation of the Rosso Ammonitico (Mid-Late Jurassic, Verona Area, Italy). Astrobiology 8: 841–857.PubMedCrossRefGoogle Scholar
  58. Préat, A., El Hassani, A. and Mamet, B. (2008b) Iron bacteria in Devonian carbonates (Tafilalt, Anti-Atlas, Morocco). Facies 54: 107–120.CrossRefGoogle Scholar
  59. Schoemann, V., de Jong, J.T.M., Lannuzel, D., Tison, J.-L., Dellile, B., Chou, L., Lancelot, C. and Becquevort, S. (2008) Microbiological control on the cycling of Fe and its isotopes in Antarctic sea ice. Geochim. Cosmochim. Acta 72(12): A209.Google Scholar
  60. Severmann, S., Johnson, C.M., Beard, B.L. and McManus, J. (2006) The effect of early diagenesis on the Fe isotope compostions of porewaters and authigenic minerals in continental margin sediments. Geochim. Cosmochim. Acta 70: 2006–2022.CrossRefGoogle Scholar
  61. Shiel, A.E., Barling, J., Orian, K.J. and Weis, D. (2009) Matrix effects on the multi-collector inductively coupled plasma mass spectrometric analysis of high-precision cadmium and zinc isotopes. Anal. Chim. Acta 633: 29–37.PubMedCrossRefGoogle Scholar
  62. Staubwasser, M., von Blanckenburg, F. and Schoenberg, R. (2006) Iron isotopes in the early marine diagenetic iron cycle. Geology 34: 629–632.CrossRefGoogle Scholar
  63. Taylor, P.D.P., Maeck, R. and De Bièvre, P. (1992) Determination of the absolute isotopic composition and atomic weight of a reference sample of natural iron. Int. J. Mass Spectrom. 121: 111–125.CrossRefGoogle Scholar
  64. Teutsch, N., von Gunten, U., Porcelli, D., Cirpka, Q.A. and Halliday, A.N. (2005) Adsorption as a cause for iron isotope fractionation in reduced groundwater. Geochim. Cosmochim. Acta 69: 4175–4185.CrossRefGoogle Scholar
  65. Thorsen, M.S. (1998) Microbial activity, oxygen status and fermentation in the gut of the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Mar. Biol. 132: 423–433.CrossRefGoogle Scholar
  66. Thorsen, M.S., Wieland, A., Ploug, H., Kragelund, C. and Nielsen, P.H. (2003) Distribution, identity and activity of symbiotic bacteria in anoxic aggregates from the hindgut of the sea urchin Echinocardium cordatum. Ophelia 57: 1–12.CrossRefGoogle Scholar
  67. van Houten, F.B. (1961) Climate significance of red beds, In: A.E.M. Nairn (ed.) Descriptive Paleoclimatology. Interscience, New York, pp. 89–139.Google Scholar
  68. van Houten, F.B. (1973) Origin of red beds. A review. Annu. Rev. Earth Planet. Sci. 1: 39–61.CrossRefGoogle Scholar
  69. Walker, T.R., Ribbe, P.H. and Hoena, R.M. (1967) Geochemistry of hornblende alteration in Pliocene red beds, Baja California, Mexico. Geol. Soc. Am. Bull. 78: 1055–1060.Google Scholar
  70. Wasylenki, L.E., Anbar, A.D., Liermann, L.J., Mathur, R., Gordon, G.W. and Brantley, S.L. (2007) Isotope fractionation during microbial metal uptake measured by MC-ICP-MS. J. Anal. Atom. Spectrom. 22: 905–910.CrossRefGoogle Scholar
  71. Williams, H.M., McCammon, C.A., Peslier, A.H., Halliday, A.N., Teutsch, N., Levasseur, S. and Burg, J.-P. (2004) Iron isotope fractionation and the oxygen fugacity of the mantle. Science 304: 1656–1659.PubMedCrossRefGoogle Scholar
  72. Zengh, Y., Anderson, R.F., Van Geen, A. and Kuwabara, J. (2000) Authigenic molybdenum formation in marine sediments: a link to porewater sulfide in the Santa Barbara Basin. Geochim. Cosmochim. Acta 64: 4165–4178.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Alain R. Préat
    • 1
    Email author
  • Jeroen T. M. De Jong
    • 1
  • Chantal De Ridder
    • 2
  • David C. Gillan
    • 3
  1. 1.Department of Earth and Environmental SciencesUniversité Libre de BruxellesBrusselsBelgium
  2. 2.Department of Marine BiologyUniversité Libre de BruxellesBrusselsBelgium
  3. 3.Department of BiologyMons UniversityMonsBelgium

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