The Biogeochemical Cycle of Silicon in the Ocean
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In the biogeochemical dynamics of marine ecosystems, silicon is a major element whose role has, for a long time, been underestimated. It is however indispensable to the activity of several biomineralizing marine organisms, some of which play an essential role in the biological pump of oceanic carbon.
This book presents notions indispensable to the knowledge on the silicon biogeochemical cycle in ocean systems, first of all describing the main quantitative analysis techniques and examination of the major organisms involved in the cycle. The author then moves on to study the most up-to-date processes to control the use of silicon and its regeneration in natural conditions, before mentioning the central role played by this original element in the control of all the biogeochemical cycles in the global ocean. The available information finally enables the global biogeochemical budget of silicon in the marine environment to be quantified.
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The Biogeochemical Cycle of Silicon in the Ocean - Bernard Quéguiner
Table of Contents
Cover
Title
Copyright
Preface
1 The Chemical Forms of Silicon in the Marine Domain
1.1. The element silicon
1.2. Orthosilicic acid
1.3. Particulate silicas
2 Techniques for Studying Stocks and Fluxes
2.1. Techniques for the chemical analysis of silicon
2.2. Techniques for the analysis of silicon fluxes
2.3. Silica deposit labeling and cellular imaging
2.4. Isotopic fractionation of silicon and utilization of δ³⁰ Si as a tracer in oceanography
3 The Marine Producers of Biogenic Silica
3.1. Radiolarians
3.2. Silicoflagellates
3.3. Diatoms
3.4. Silicification within the scope of nanoplankton and picoplankton
3.5. Siliceous sponges
3.6. The functions of biogenic silica
3.7. The evolution of the siliceous organisms and the oceanic cycle of the silicon
3.8. Sedimentary opal deposits
4 Cellular Mechanisms of Silica Deposition by Diatoms
4.1. Influence of orthosilicic acid availability on uptake and diatom growth
4.2. The chemical form of dissolved Si available for diatoms
4.3. Cellular mechanisms of orthosilicic acid uptake
4.4. Intervention of specific proteins in the deposition mechanism
4.5. The stoichiometric ratios Si/C/N of diatoms
5 Dissolution of Biogenic Silica and Orthosilicic Acid Regeneration
5.1. Reactivity of the particulate silica and dissolution constants
5.2. Processes of control of the dissolution in aqueous phase
5.3. The solubility of opal in natural conditions
6 The Control of Biogeochemistry by Silicon at Global Scale
6.1. The preservation of calcite in ocean sediments
6.2. The central role of the Southern Ocean
6.3. The silicic acid leakage hypothesis (SALH)
7 The Global Budget of Silicon in the Oceans
7.1. Estimates of production and export of biogenic silica
7.2. The biogeochemical cycle of silicon in the Global Ocean
Bibliography
Index
End User License Agreement
List of Tables
1 The Chemical Forms of Silicon in the Marine Domain
Table 1.1. Natural atomic masses and abundances of three stable isotopes of silicon [HAY 16]. The weighted average atomic mass of natural silicon is equal to 28.08549871
4 Cellular Mechanisms of Silica Deposition by Diatoms
Table 4.1. Values of the half-saturation constants
KSi calculated for different potential substrates present at the pH values tested in Phaeodactylum tricornutum [RIE 85]
5 Dissolution of Biogenic Silica and Orthosilicic Acid Regeneration
Table 5.1. Values of the rate constants of silica in seawater (at 25°C and pH 8.0–8.4) for various mineral forms (from Wollast, [WOL 74])
Table 5.2. Variability of the specific surface area for various types of siliceous materials
7 The Global Budget of Silicon in the Oceans
Table 7.1. Early estimations of biogenic silica production in surface waters of the Global Ocean (Tmol = teramol = 10¹² mol)
Table 7.2. Silicon balance in the Global Ocean (modified according to Tréguer and De La Rocha [TRÉ 13])
List of Illustrations
1 The Chemical Forms of Silicon in the Marine Domain
Figure 1.1. Relative distribution of the majority of the chemically dissolved species of silicon under thermodynamic conditions comparable to seawater (0.6 M NaCl, 25ºC) as a function of the pH of the solution
Figure 1.2. Structural model of biogenic silica. Al enters the network structure while preserving the three-dimensional environment resulting from sharing tetrahedra SiO4. The substitution of Si⁴+ + by Al³+ generates a negative charge. Chemical analysis of the diatom frustule suggests charge compensation by Ca²+ cations [GEH 02]
2 Techniques for Studying Stocks and Fluxes
Figure 2.1. Typical extraction kinetics of particulate silica. The first part of the curve represents the dissolution of the BSi (high-dissolution rate), while the linear phase reached at the end of extraction corresponds to the dissolution phase of LSi (at a theoretically much lower dissolution rate in an alkaline medium). The correction is to draw the tangent to the linear portion of the curve. The extrapolated intercept at time t0 equals the corrected biogenic silica content of the sample
Figure 2.2. Extraction kinetics of silicon a) and aluminum b) from a sediment sample from Tokyo Bay under various alkaline conditions (●: 0.2 N NaOH; ο: 0.1 N NaOH; ▲: 0.5 M Na2CO3; △: 0.1 M Na2CO3). The linear relationship between these two elements c) enables us to calculate the amount of biogenic silica of the sample (intercept of the line on the y-axis) as corrected from the interference of the lithogenic silica. The slope of the regression line represents the Si/Al ratio of the lithogenic material (according to [KAM 00])
Figure 2.3. Principle of the determination of the production of silica and phosphorus. Evolution of the activity of ³²P and of ³²Si in the diatoms after the incubation (from [LEY 93])
Figure 2.4. a) Visualization with microautoradiography of the synthesis of intercalary bands in Rhizosolenia debyana (scale: 20 μm) [SHI 99]. b) Labeling of a chain of Rhizosolenia styliformis by PDMPO (scale: 100 μm, photograph from M. Lasbleiz)
Figure 2.5. Simulation of silicon isotopic fractionation related to the precipitation of the biogenic silica (bSiO2) by diatoms in a closed system (Rayleigh distillation) and in an open system at equilibrium. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
3 The Marine Producers of Biogenic Silica
Figure 3.1. Different morphological types of siliceous endoskeleton of radiolarians [BOL 99]
Figure 3.2. Structure of the endoskeleton of the present silicoflagellate, Distephanus speculum [CAR 07]
Figure 3.3. General and microarchitectural form of the frustule of a centric diatom: a) image of Coscinodiscus sp. from a scanning electronic microscope (SEM); b) detail of the field delimited in Figure a); c) diagram of the three-dimensional organization of the frustule (according to [GOR 09])
Figure 3.4. Observation of the Parmales Triparma cf. laevis by SEM, according to Ichinomiya et al. [ICH 11]. Scale: 1 µm
Figure 3.5. Form and microarchitecture of the choanoflagellate Acanthoeca spectabilis (p: protoplasm located at the base of the lorica formed by the edges of biogenic silica). Observed by a transmission electronic microscope by Marchant and Perrin [MAR 90]
Figure 3.6. Examples of the morphology of spicules in Demospongiae (according to [URI 03])
Figure 3.7. Estimation of average marine orthosilicic acid concentration during the Neoproterozoic and the Phanerozoic: according to Siever [SIE 91]; incorporating the data from Siever [SIE 92] and Grenne and Slack [GRE 03]. The red arrows correspond to the successive emergences of radiolarians, sponge and diatoms. The graph on the right shows the decrease of H4SiO4 concentration attributable to diatoms. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
Figure 3.8. Distribution (% with regard to dry weight of the sediment) of total organic carbon: a) the carbonates; b) the opal; c) for all the data from the Pangea database [DIT 05], and comparison with respective outputs (d, e, f) from the coupled OGCM/Biogeochemistry model PISCES [GEH 06]. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
4 Cellular Mechanisms of Silica Deposition by Diatoms
Figure 4.1. Comparison of the theoretical kinetics of uptake and growth in diatoms. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
Figure 4.2. Schematic representation of the components of the transmembrane transport of mineral nutrients. The low affinity component represents a passive diffusion process. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
Figure 4.3. Model proposed by Bhattacharyya and Volcano [BHA 80] for the Na+–K+-dependent uptake of orthosilicic acid in the marine apochlorotic diatom Nitzschia alba
Figure 4.4. Various elements of frustule diatom silicification and sequence of events during the cell cycle: 1) shortly before the cell division, the frustule has a maximum of intercalary bands; 2) biogenic silica deposits within the silica deposition vesicle (SDV) of each daughter cell immediately after cytokinesis; 3) SDVs gradually extend as the deposit of biogenic silica proceeds and new valves are synthesized; 4) at the final stage of development of SDVs, each one contains a whole new hypotheca; 5) the new valves are deposited in cleavage furrow of daughter cells by exocytosis of SDV; 6) the daughter cells separate; 7) expansion of protoplasm at the interphase requires the deposition of intercalary bands inside new SDVs; 8) expansion of protoplasm at the interphase and the deposition of intercalary bands continues; 9) after the synthesis of the pleural band, the increase in cell volume stops and DNA replication starts, according to Kröger and Poulsen [KRO 08]. For a color version of the figure, see www.iste.co.uk/queguiner/silicon.zip
Figure 4.5. Orthosilicic acid uptake, changes in cell concentration and transport rate of dissolved silicon in the absence (○) or after addition of 10 µg mL-1 cycloheximide (●) on a synchronous culture of Navicula pelliculosa (synchronization obtained by a day/night cycle of 5/7 h) – according to Sullivan [SUL 77]
Figure 4.6. Condensation reaction between orthosilicic acid and serine on the protein template. Water molecules resulting from the condensation may be removed or incorporated into the frustule through hydrogen bonds with the oxygen atoms of the silica (according to [HEC 73])
Figure 4.7. Structural model of the organic layers of diatom cell wall. The polysaccharide outer layer is composed of various sugars: Gl, glucose; M, mannose; Fu, fucose; Xy, xylose. The protein template residues are Ser, serine; Gly, glycine; Thr, threonine; Asp: aspartic acid (according to [HEC 73])
Figure 4.8. Electron microscopy analysis of biogenic silica and organic material included in frustules of Thalassiosira pseudonana and resistant to attack by ammonium fluoride (from Scheffel et al. [SCH 11]): a) overview of resistant organic material; b) detail of an annular organic matrix; c) intact biogenic silica of a frustule of Thalassiosira pseudonana (dotted white lines delineate the non-perforated edge zones of intercalary bands. V: valve, Gb, intercalary bands of the cingulum)
Figure 4.9. Orthosilicic acid uptake kinetics by natural populations of diatoms under different concentrations of dissolved iron in the Polar Front area of the Southern Ocean, Australian sector (53° 48’S, 141° 53’E); a) in the surface layer (20 m, [Fe] <0.07 nM); b) at the depth of biogenic silica maximum (105 m, [Fe] around 0.13 nM); c) profile of dissolved iron concentrations. a) and b) according to Quéguiner [QUÉ 01]; c) according to Sedwick et al. [SED 99])
5 Dissolution of Biogenic Silica and Orthosilicic Acid Regeneration
Figure 5.1. Changes in silica solubility with the depth from data presented by Willey [WIL 74] and Dixit et al. [DIX 01]. (Ce)z: solubility at depth z; (Ce)0: solubility in surface waters
Figure 5.2. Frustule dissolution kinetics of the freshwater diatom Navicula pelliculosa at different pH conditions (redrawn from Lewin [LEW 61]) at 19°C. The pH decreases related to the increase of orthosilicic acid concentration in the course of the experiments are shown on the different curves
Figure 5.3. Biogenic silica dissolution versus time at different temperatures in two species of centric diatoms: a) Coscinodiscus gigas; b) Eucampia zodiacus) according to Kamatani[ KAM 82]. The first-order specific rate is determined by the slope of the relation described by equation [5.10]
Figure 5.4. Relationship between the specific dissolution rate (K) and temperature for different types of material: 1) Skeletonema costatum; 2) Chaetoceros gracilis; 3) Thalassiosira decipiens; 4) centric diatom; 5) diatom communities; 6) Eucampia zodiacus; and 7) Coscinodiscus gigas (according to Kamatani, [KAM 82])
Figure 5.5. Increase in the concentrations of H4SiO4 dissolved from