Geo-Marine Letters

, Volume 30, Issue 5, pp 477–492 | Cite as

Microbial mediation of benthic biogenic silica dissolution

Original

Abstract

Pore water profiles from 24 stations in the South Atlantic (located in the Guinea, Angola, Cape, Guyana, and Argentine basins) show good correlations of oxygen and silicon, suggesting microbially mediated dissolution of biogenic silica. We used simple analytical transport and reaction models to show the tight coupling of the reconstructed process kinetics of aerobic respiration and silicon regeneration. A generic transport and reaction model successfully reproduced the majority of Si pore water profiles from aerobic respiration rates, confirming that the dissolution of biogenic silica (BSi) occurs proportionally to O2 consumption. Possibly limited to well-oxygenated sediments poor in BSi, benthic Si fluxes can be inferred from O2 uptake with satisfactory accuracy. Compared to aerobic respiration kinetics, the solubility of BSi emerged as a less influential parameter for silicon regeneration. Understanding the role of bacteria for silicon regeneration requires further investigations, some of which are outlined. The proposed aerobic respiration control of benthic silicon cycling is suitable for benthic–pelagic models. The empirical relation of BSi dissolution to aerobic respiration can be used for regionalization assessments and estimates of the silicon budget to increase the understanding of global primary and export production patterns.

Notes

Acknowledgements

Constructive comments and suggestions by Bernard P. Boudreau, Gunnar Brandt, and two anonymous reviewers are greatly acknowledged. We thank Kerstin Pfeifer, Katherina Seiter, and Matthias Zabel for fruitful discussions on the subject. Special thanks go to Frank Wenzhöfer and Matthias Zabel for supplying in situ O2 and Mn data. This work was supported by the DFG projects FOR 432 and SFB 754.

References

  1. Adler M, Hensen C, Schulz HD (2000) CoTReM - Column Transport and Reaction Model. Version 2.3, User Guide. Faculty of Geochemistry, University of BremenGoogle Scholar
  2. Adler M, Hensen C, Wenzhöfer F, Pfeifer K, Schulz HD (2001) Modeling of calcite dissolution by oxic respiration in supralysoclinal deep-sea sediments. Mar Geol 177:167–189CrossRefGoogle Scholar
  3. Archer D, Lyle M, Rodgers K, Froelich P (1993) What controls opal preservation in tropical deep-sea sediments? Paleoceanography 8:7–21CrossRefGoogle Scholar
  4. Armstrong RA, Lee C, Hedges JI, Honjo S, Wakeham SG (2002) A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep-Sea Res II 49:219–236CrossRefGoogle Scholar
  5. Barker P, Fontes JC, Gasse F, Druart JC (1994) Experimental dissolution of diatom silica in concentrated salt solutions and implications for paleoenvironmental reconstruction. Limnol Oceanogr 39(1):99–110CrossRefGoogle Scholar
  6. Berelson WM, Hammond DE, Johnson KS (1987) Benthic fluxes and the cycling of biogenic silica and carbon in two southern-California borderland basins. Geochim Cosmochim Acta 51:1345–1363CrossRefGoogle Scholar
  7. Berelson WM, Prokopenko M, Sansone FJ, Graham AW, McManus J, Bernhard JM (2005) Anaerobic diagenesis of silica and carbon in continental margin sediments: discrete zones of TCO2 production. Geochim Cosmochim Acta 69:4611–4629CrossRefGoogle Scholar
  8. Berner RA (1980) Early diagenesis: a theoretical approach. Princton University Press, PrinctonGoogle Scholar
  9. Bidle KD, Azam F (1999) Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397:508–512CrossRefGoogle Scholar
  10. Bidle KD, Azam F (2001) Bacterial control of silicon regeneration from diatom detritus: significance of bacterial ectohydrolases and species identity. Limnol Oceanogr 46:1606–1623CrossRefGoogle Scholar
  11. Bidle KD, Manganelli M, Azam F (2002) Regulation of oceanic silicon and carbon preservation by temperature control on bacteria. Science 298:1980–1984CrossRefGoogle Scholar
  12. Boudreau BP (1990a) Asymptotic forms and solutions of the model for silica-opal diagenesis in bioturbated sediments. J Geophys Res Oceans 95:7367–7379CrossRefGoogle Scholar
  13. Boudreau BP (1990b) Modeling early diagenesis of silica in non-mixed sediments. Deep-Sea Res A 37:1543–1567CrossRefGoogle Scholar
  14. Boudreau BP (1997) Diagenetic models and their implementation. Modelling transport and reactions in aquatic sediments. Springer, BerlinGoogle Scholar
  15. Canfield DE, Jorgensen BB, Fossing H, Glud R, Gundersen J, Ramsing NB, Thamdrup B, Hansen JW, Nielsen LP, Hall POJ (1993) Pathways of organic-carbon oxidation in 3 continental-margin sediments. Mar Geol 113:27–40CrossRefGoogle Scholar
  16. DeMaster DJ (1981) The supply and accumulation of silica in the marine-environment. Geochim Cosmochim Acta 45:1715–1732CrossRefGoogle Scholar
  17. DeMaster DJ (2002) The accumulation and cycling of biogenic silica in the southern ocean: revisiting the marine silica budget. Deep-Sea Res II 49:3155–3167CrossRefGoogle Scholar
  18. Devol AH, Christensen JP (1993) Benthic fluxes and nitrogen cycling in sediments of the continental margin of the eastern North Pacific. J Mar Res 51:345–372CrossRefGoogle Scholar
  19. Dixit S, Van Cappellen P (2002) Surface chemistry and reactivity of biogenic silica. Geochim Cosmochim Acta 66:2559–2568CrossRefGoogle Scholar
  20. Dixit S, Van Cappellen P (2003) Predicting benthic fluxes of silicic acid from deep-sea sediments. J Geophys Res Oceans 108(C10):3334. doi:10.1029/2002JC001309 CrossRefGoogle Scholar
  21. 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 73:333–352CrossRefGoogle Scholar
  22. Dugdale RC, Wilkerson FP (1998) Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391:270–273CrossRefGoogle Scholar
  23. Dugdale RC, Wilkerson FP, Minas HJ (1995) The role of a silicate pump in driving new production. Deep-Sea Res I 42:697–719CrossRefGoogle Scholar
  24. Egge JK, Aksnes DL (1992) Silicate as regulating nutrient in phytoplankton competition. Mar Ecol 83:281–289CrossRefGoogle Scholar
  25. Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, Dauphin P, Hammond D, Hartman B, Maynard V (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic—suboxic diagenesis. Geochim Cosmochim Acta 43:1075–1090CrossRefGoogle Scholar
  26. Gallinari M, Ragueneau O, Corrin L, DeMaster DJ, Tréguer P (2002) The importance of water column processes on the dissolution properties of biogenic silica in deep-sea sediments i. solubility. Geochim Cosmochim Acta 66:2701–2717CrossRefGoogle Scholar
  27. Gallinari M, Ragueneau O, DeMaster D, Hartnett H, Rickert D, Thomas C (2008) Influence of seasonal phytodetritus deposition on biogenic silica dissolution in marine sediments–Potential effects on preservation. Deep-Sea Res II 55(22/23):2451–2464CrossRefGoogle Scholar
  28. Gehlen M, Beck L, Calas G, Flank AM, Van Bennekom AJ, Van Beusekom JEE (2002) Unraveling the atomic structure of biogenic silica: evidence of the structural association of Al and Si in diatom frustules. Geochim Cosmochim Acta 66:1601–1609CrossRefGoogle Scholar
  29. Glud RN, Gundersen JK, Jørgensen BB, Revsbech NP, Schulz HD (1994) Diffusive and total uptake of deep-sea sediments in the eastern South Atlantic Ocean: In situ and laboratory measurements. Deep-Sea Res I 41:1767–1788CrossRefGoogle Scholar
  30. Goel R, Mino T, Satoh H, Matsuo T (1998) Comparison of hydrolytic enzyme systems in pure culture and activated sludge under different electron acceptor conditions. Water Sci Technol 37(4/5):335–343Google Scholar
  31. Greenwood JE, Truesdale VW, Rendell AR (2001) Biogenic silica dissolution in seawater—in vitro chemical kinetics. Prog Oceanogr 48:1–23CrossRefGoogle Scholar
  32. Hall POJ, Hulth S, Hulthe G, Landen A, Tengberg A (1996) Benthic nutrient fluxes on a basin-wide scale in the Skagerrak (north-eastern North Sea). J Sea Res 35:123–137CrossRefGoogle Scholar
  33. Hammond DE, McManus J, Berelson WM, Kilgore TE, Pope RH (1996) Early diagenesis of organic material in equatorial Pacific sediments: stoichiometry and kinetics. Deep-Sea Res II 43:1365–1412CrossRefGoogle Scholar
  34. Hecky RE, Mopper K, Kilham P, Degens ET (1973) The amino acid and sugar composition of diatom cell-walls. Mar Biol 19:323–331CrossRefGoogle Scholar
  35. Hedges JI, Baldock JA, Gelinas Y, Lee C, Peterson M, Wakeham SG (2001) Evidence for non-selective preservation of organic matter in sinking marine particles. Nature 409:801–804CrossRefGoogle Scholar
  36. Hensen C, Landenberger H, Zabel M, Schulz HD (1998) Quantification of diffusive benthic fluxes of nitrate, phosphate, and silicate in the southern Atlantic Ocean. Glob Biogeochem Cycles 12:193–210CrossRefGoogle Scholar
  37. Hensen C, Zabel M, Schulz HD (2000) A comparison of benthic nutrient fluxes from deep-sea sediments off Namibia and Argentina. Deep-Sea Res II 47:2029–2050CrossRefGoogle Scholar
  38. Hensen C, Zabel M, Pfeifer K, Schwenk T, Kasten S, Riedinger N, Schulz HD, Boettius A (2003) Control of sulfate pore-water profiles by sedimentary events and the significance of anaerobic oxidation of methane for the burial of sulfur in marine sediments. Geochim Cosmochim Acta 67:2631–2647CrossRefGoogle Scholar
  39. Henze M, Mladenovski C (1991) Hydrolysis of particulate substrate by activated sludge under aerobic, anoxic and anaerobic conditions. Water Res 25(1):61–64CrossRefGoogle Scholar
  40. Jahnke RA (1996) The global ocean flux of particulate organic carbon: areal distribution and magnitude. Glob Biogeochem Cycles 10:71–88CrossRefGoogle Scholar
  41. Jin X, Gruber N, Dunne JP, Sarmiento JL, Armstrong RA (2006) Diagnosing the contribution of phytoplankton functional groups to the production and export of particulate organic carbon, CaCO3, and opal from global nutrient and alkalinity distributions. Globb Biogeochem Cycles 20. doi:10.1029/2005GB002532 Google Scholar
  42. Kamatani A, Ejiri N, Tréguer P (1988) The dissolution kinetics of diatom ooze from the Antarctic area. Deep-Sea Res A 35:1195–1203CrossRefGoogle Scholar
  43. Keir RS (1982) Dissolution of calcite in the deep-sea—theoretical prediction for the case of uniform size particles settling into a well-mixed sediment. Am J Sci 282:193–236CrossRefGoogle Scholar
  44. Khalil K, Rabouille C, Gallinari M, Soetaert K, DeMaster D, Ragueneau O (2007) Constraining biogenic silica dissolution in marine sediments: a comparison between diagenetic models and experimental dissolution rates. Mar Chem 106(1/2):223–238CrossRefGoogle Scholar
  45. Kröger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298:584–586CrossRefGoogle Scholar
  46. Landenberger H, Adler M, Zabel M, Hensen C, Schulz HD (1997) Softwareentwicklung zur computerunterstützten Simulation frühdiagenetischer Prozesse in marinen Sedimenten. Z Dtsch Geol Ges 148:447–455Google Scholar
  47. Lee C, Wakeham SG, Hedges JI (2000) Composition and flux of particulate amino acids and chloropigments in equatorial Pacific seawater and sediments. Deep-Sea Res I 47:1535–1568CrossRefGoogle Scholar
  48. Lewin JC (1961) The dissolution of silica from diatom walls. Geochim Cosmochim Acta 21:182–198CrossRefGoogle Scholar
  49. Luce RW, Bartlett RW, Parks GA (1972) Dissolution kinetics of magnesium silicates. Geochim Cosmochim Acta 36:35–50CrossRefGoogle Scholar
  50. Mann DG (1999) The species concept in diatoms. Phycologia 38:437–495CrossRefGoogle Scholar
  51. Martin WR, Bender M, Leinen M, Orchardo J (1991) Benthic organic-carbon degradation and biogenic silica dissolution in the central equatorial Pacific. Deep-Sea Res A 38:1481–1516CrossRefGoogle Scholar
  52. McManus J, Hammond DE, Berelson WM, Kilgore TE, DeMaster DJ, Ragueneau OG, Collier RW (1995) Early diagenesis of biogenic opal—dissolution rates, kinetics, and paleoceanographic implications. Deep-Sea Res II 42:871–903CrossRefGoogle Scholar
  53. Michalopoulos P, Aller RC (2004) Early diagenesis of biogenic silica in the Amazon delta: alteration, authigenic clay formation, and storage. Geochim Cosmochim Acta 68:1061–1085CrossRefGoogle Scholar
  54. Michalopoulos P, Aller RC, Reeder RJ (2000) Conversion of diatoms to clays during early diagenesis in tropical, continental shelf muds. Geology 28:1095–1098CrossRefGoogle Scholar
  55. Moriceau B, Goutx M, Guigue C, Lee C, Armstrong R, Duflos M, Tamburini C, Charrière B, Ragueneau O (2009) Si-C interactions during degradation of the diatom Skeletonema marinoi. Deep-Sea Res II 56(18):1381–1395CrossRefGoogle Scholar
  56. Müller PJ, Schneider R (1993) An automated leaching method for the determination of opal in sediments and particulate matter. Deep-Sea Res I 40:425–444CrossRefGoogle Scholar
  57. Murray RW, Leinen M (1993) Chemical transport to the seafloor of the equatorial Pacific Ocean across a latitudinal transect at 135°W: tracking sedimentary major, trace, and rare earth element fluxes at the Equator and the Intertropical Convergence Zone. Geochim Cosmochim Acta 57(17):4141–4163CrossRefGoogle Scholar
  58. Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean—revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycles 9:359–372CrossRefGoogle Scholar
  59. Pfeifer K, Hensen C, Adler M, Wenzhöfer F, Weber B, Schulz HD (2002) Modeling of subsurface calcite dissolution, including the respiration and reoxidation processes of marine sediments in the region of equatorial upwelling off Gabon. Geochim Cosmochim Acta 66:4247–4259CrossRefGoogle Scholar
  60. Picket-Heaps J, Tippit DH, Andreozzi JA (1990) The cell biology of diatom valve formation. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 7. Biopress, Bristol, pp 1–168Google Scholar
  61. Rabouille C, Gaillard JF, Tréguer P, Vincendeau MA (1997) Biogenic silica recycling in surficial sediments across the Polar Front of the Southern Ocean (Indian Sector). Deep-Sea Res I 44:1151–1176Google Scholar
  62. Ragueneau O, Tréguer P, Leynaert A, Anderson RF, Brzezinski MA, DeMaster DJ, Dugdale RC, Dymond J, Fischer G, Francois R, Heinze C, Maier-Reimer E, Martin-Jezequel V, Nelson DM, Queguiner B (2000) A review of the Si cycle in the modern ocean: recent progress and missing gaps in the application of biogenic opal as a paleoproductivity proxy. Glob Planet Change 26:317–365CrossRefGoogle Scholar
  63. Ragueneau O, Dittert N, Pondaven P, Tréguer P, Corrin L (2002) Si/C decoupling in the world ocean: Is the Southern Ocean different? Deep-Sea Res II 49:3127–3154CrossRefGoogle Scholar
  64. Rickert D, Schlüter M, Wallmann K (2002) Dissolution kinetics of biogenic silica from the watercolumn to the sediments. Geochim Cosmochim Acta 66:439–455CrossRefGoogle Scholar
  65. Rivkin RB, Legendre L, Deibel D, Tremblay JE, Klein B, Crocker K, Roy S, Silverberg N, Lovejoy C, Mesple F, Romero N, Anderson MR, Matthews P, Savenkoff C, Vezina A, Therriault JC, Wesson J, Berube C, Ingram RG (1996) Vertical flux of biogenic carbon in the ocean: is there food web control? Science 272:1163–1166CrossRefGoogle Scholar
  66. Romero O, Hensen C (2002) Oceanographic control of biogenic opal and diatoms in surface sediments of the Southwestern Atlantic. Mar Geol 186:263–280CrossRefGoogle Scholar
  67. Rothman DH, Forney DC (2007) Physical model for the decay and preservation of marine organic carbon. Science 316:1325–1328CrossRefGoogle Scholar
  68. Sayles FL, Deuser WG, Goudreau JE, Dickison WH, Jickells TD, King P (1996) The benthic cycle of biogenic opal at the Bermuda Atlantic Time Series site. Deep-Sea Res I 43:383–409CrossRefGoogle Scholar
  69. Schink DR, Guinasso NL, Fanning KA (1975) Processes affecting concentration of silica at sediment-water interface of Atlantic Ocean. J Geophys Res Oceans Atmospheres 80:3013–3031CrossRefGoogle Scholar
  70. Schrader HJ (1971) Fecal pellets: role in sedimentation of pelagic diatoms. Science 174:55–57CrossRefGoogle Scholar
  71. Seiter K, Hensen C, Schroter E, Zabel M (2004) Organic carbon content in surface sediments—defining regional provinces. Deep-Sea Res I 51:2001–2026CrossRefGoogle Scholar
  72. Tande K, Slagstad D (1985) Assimilation efficiency in herbivorous aquatic organisms—the potential of the ratio methods using 14C and biogenic silica as markers. Limnol Oceanogr 30:1093–1099CrossRefGoogle Scholar
  73. Thamdrup B, Canfield DE (1996) Pathways of carbon oxidation in continental margin sediments off central Chile. Limnol Oceanogr 41:1629–1650CrossRefGoogle Scholar
  74. Tréguer P, Nelson DM, Van Bennekom AJ, Demaster DJ, Leynaert A, Queguiner B (1995) The silica balance in the world ocean—a reestimate. Science 268:375–379CrossRefGoogle Scholar
  75. Truesdale VW, Greenwood JE, Rendell AR (2005) In vitro, batch-dissolution of biogenic silica in seawater—the application of recent modelling to real data. Progr Oceanogr 66(1):1–24CrossRefGoogle Scholar
  76. Van Bennekom AJ, Buma AGJ, Nolting RF (1991) Dissolved aluminum in the Weddell-Scotia confluence and effect of Al on the dissolution kinetics of biogenic silica. Mar Chem 35:423–434CrossRefGoogle Scholar
  77. Van Beusekom JEE, Van Bennekom AJ, Tréguer P, Morvan J (1997) Aluminium and silicic acid in water and sediments of the Enderby and Crozet Basins. Deep-Sea Res II 44:987–1003CrossRefGoogle Scholar
  78. Van Cappellen P, Qiu LQ (1997a) Biogenic silica dissolution in sediments of the Southern Ocean. 1. Solubility. Deep-Sea Res II 44:1109–1128CrossRefGoogle Scholar
  79. Van Cappellen P, Qiu LQ (1997b) Biogenic silica dissolution in sediments of the Southern Ocean. 2. Kinetics. Deep-Sea Res II 44:1129–1149CrossRefGoogle Scholar
  80. Van Cappellen P, Dixit S, Van Beusekom J (2002) Biogenic silica dissolution in the oceans: reconciling experimental and field-based dissolution rates. Glob Biogeochem Cycles 16(4), 1075. doi:10.1029/2001GB001431 CrossRefGoogle Scholar
  81. Vetter YA, Deming JW, Jumars PA, Krieger-Brockett BB (1998) A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36:75–92CrossRefGoogle Scholar
  82. Volcani BE (2002) Cell wall formation in diatoms: morphogenesis and biochemistry. In: Simpson TL, Volcani, BE (eds) Silicon and siliceous structures in biological systems. Springer, Berlin, pp 157–200Google Scholar
  83. Wenzhöfer F, Glud RN (2002) Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade. Deep-Sea Res I 49:1255–1279CrossRefGoogle Scholar
  84. Wenzhöfer F, Adler M, Kohls O, Hensen C, Strotmann B, Schulz HD (2001) Calcite dissolution driven by benthic mineralization in the deep-sea: In situ measurements of Ca2 + , pH, pCO2 and O2. Geochim Cosmochim Acta 65:2677–2690CrossRefGoogle Scholar
  85. Wetherbee R, Crawford S, Mulvaney P (2000) The nanostructure and development of diatom biosilica. In: Baeurlein E (ed) Biomineralization: from biology to biotechnology and medical application. Wiley-VCH, Weinheim, pp 189–206Google Scholar
  86. Zabel M, Dahmke A, Schulz HD (1998) Regional distribution of diffusive phosphate and silicate fluxes through the sediment water interface—The eastern South Atlantic. Deep-Sea Res I 45:277–300CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Institute for Chemistry and Biology of the Marine Environment (ICBM)University of OldenburgOldenburgGermany
  2. 2.Leibniz-Institut für MeereswissenschaftenIFM-GEOMARKielGermany

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