Hydrobiologia 426: 1–24, 2000. G. Liebezeit, S. Dittmann & I. Kröncke (eds), Life at Interfaces and Under Extreme Conditions. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
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Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals Erik Kristensen Institute of Biology, Odense University, SDU, DK-5230 Odense M, Denmark E-mail:
[email protected] Key words: oxic/anoxic interfaces, diagenesis, carbon, oxygen, bioturbation, irrigation
Abstract The present paper reviews the current knowledge on diagenetic carbon transformations at the oxic/anoxic interface in coastal marine sediments. Oxygen microelectrodes have revealed that most coastal sediments are covered only by a thin oxic surface layer. The penetration depth of oxygen into sediments is controlled by the balance between downward transport and consumption processes. Consumption of oxygen is directly or indirectly caused by respiration of benthic organisms. Aerobic organisms have the enzymatic capacity for complete oxidation of organic carbon. Anaerobic decay occurs stepwise, involving several types of bacteria. Large organic molecules are first fermented into small moieties. These are then oxidized completely by anaerobic respirers using a sequence of electron acceptors: Mn4+ , NO3 − , Fe3+ , SO4 2− and CO2 . The quantitative role of each electron acceptor depends on the sediment type and water depth. Since most of the sediment oxygen uptake is due to reoxidation of reduced metabolites, aerobic respiration is of limited importance. It has been suggested that sediments contain three major organic fractions: (1) fresh material that is oxidized regardless of oxygen conditions; (2) oxygen sensitive material that is only degraded in the presence of oxygen; and (3) totally refractory organic matter. Processes occurring at the oxic/anoxic boundaries are controlled by a number of factors. The most important are: (1) temperature, (2) organic supply, (3) light, (4) water currents, and (5) bioturbation. The role of bioturbation is important because the infauna creates a three-dimensional mosaic of oxic/anoxic interfaces in sediments. The volume of oxic burrow walls may be several times the volume of oxic surface sediment. The infauna increases the capacity, but not the overall organic matter decay in sediments, thus decreasing the pool of reactive organic matter. The increase in decay capacity is partly caused by injection of oxygen into the sediment, and thereby enhancing the decay of old, oxygen sensitive organic matter several fold. Finally, some future research directions to improve our understanding of diagenetic processes at the oxic/anoxic interface are suggested.
Introduction The boundary between oxic and anoxic zones is a well defined and sharp interface in most aquatic environments; particularly in the sediment. Oxygen is the energetically most favorable electron acceptor for microbial respiration (Fenchel et al., 1998), but the high consumption rate combined with low solubility in water usually prevents deep penetration of oxygen into coastal sediments. The lack of available oxygen may have serious implications for the biotic community and, thus, rates of organic matter diagenesis in sediments (Kristensen et al., 1995; Fenchel, 1996a, b).
Macrofaunal structures, such as burrows formed by bottom-dwelling animals, represent an important mosaic of physico-chemical and biological microenvironments in most coastal sediments. The surface area available for diffusive solute exchange, as well as the areas of oxic/anoxic boundaries, are considerably increased by the presence of irrigated burrows (Kristensen, 1984; Fenchel, 1996a). Accordingly, the activities of burrowing and irrigating infauna alter the one-dimensional diagenetic stratification into a threedimensional, complex and time-dependent stratification with effects on microbial communities deep in the sediment (Aller, 1982; Kristensen, 1988).
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Figure 1. Oxygen penetration into marine sediments at water column depths from 1 to about 5000 m. The horizontal line indicates the sediment–water interface. The oxygen saturation level is, for simplicity, fixed to 197 µM in all environments. Modified from Jørgensen & Revsbech (1985) and Glud et al. (1994).
The present paper reviews the current knowledge on dynamics of oxic/anoxic interfaces with respect to carbon transformations in coastal marine sediments. The distribution patterns of oxic/anoxic interfaces are discussed and related to the factors affecting the dominating oxic and anoxic diagenetic processes. The quantitative role of deep oxygen penetration caused by animal burrows on the overall rate of organic matter decomposition is evaluated. The general discussion is supplemented with relevant case studies and conceptual models. Oxygen distribution and oxic/anoxic interfaces Marine sediments are reducing environments covered only by a thin oxic surface layer. Sediments in productive shallow coastal waters are generally characterized by oxygen penetration depths of millimeters compared with cm or dm scales in oceanic sediments underlying a deep oligotrophic water column (Figure 1) (Reimers et al., 1986; Glud et al., 1994). The penetration depth of oxygen is controlled by the balance between downward transport of oxygen from above and by consumption processes of all benthic organisms and their metabolic products within the sediment. The transport of oxygen in sediments is driven
Figure 2. Hypothetical oxygen profile in a coastal marine sediment. A diffusive boundary layer of 0.3 mm thickness separates the sediment from the turbulent overlying water. The horizontal line indicates the interface between the boundary layer and the turbulent water phase. The cross-hatched horizontal bar represents the sediment–water interface.
by molecular diffusion and water currents or bioturbation induced advective forces (Huettel & Gust, 1992a), whereas the consumption processes are driven by microbially mediated oxidation of organic matter and reduced inorganic metabolites (Jørgensen, 1983). The rate of benthic oxygen uptake may be hampered by a mm thick diffusive boundary layer above the sediment–water interface (Jørgensen & Revsbech, 1985; Archer et al., 1989). The diffusive boundary layer is a viscous film of water at the sediment–water interface created by the internal friction of water close to a solid surface (Figure 2). Molecular diffusion is the principal mechanism for mass transport within the diffusive boundary layer (Santschi et al., 1983). As eddy diffusion is reduced under low water current regimes, the diffusive boundary layer can create a barrier between the sediment and the overlying water, thus reducing the oxygen concentration at the sediment surface compared with the stirred overlying water. Consequently, the thickness of the diffusive boundary layer may control the influx and penetration depth of oxygen into the sediment, particularly when oxygen uptake is high (Jørgensen & Revsbech, 1985). The oxidized zone that extends just below the upper oxic zone in sediments is frequently denoted the
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Figure 3. Idealized presentation of vertical profiles of oxidized compounds (electron acceptors) in a marine sediment. The depth of the ‘oxic’ zone is determined by the penetration of oxygen. The ‘suboxic’ zone contains a number of electron acceptors, i.e. nitrate, oxidized manganese and iron, and the position of the lower bounday is usually defined by the penetration depth of oxidized iron. Sulfate is the dominating electron acceptor in the ‘reduced’ zone. When sulfate is depleted, methane and carbon dioxide (not shown) are the dominating compounds for diagenetic processes.
‘suboxic zone’ (Froelich et al., 1979). The suboxic zone is characterized by high concentrations of oxidized inorganic compounds such as nitrate, manganese oxides and iron oxyhydroxides (Jørgensen, 1983), and appears visually as a light brown upper layer of most sediments (Figure 3). The reduced zone extends below the suboxic zone and is often characterized by the presence of sulfides produced by bacterial sulfate reduction, either in precipitated form as iron sulfides or in dissolved form as free sulfide (Chanton et al., 1987). Under conditions of high sediment oxygen uptake combined with stagnant conditions in the overlying water, the suboxic zone may disappear and the oxic/anoxic interface with free sulfide present just below the oxic zone moves upwards to the surface or even into the overlying water (Stigebrandt & Wulff, 1987; Kemp et al., 1992; Møller, 1996). Determination of oxygen penetration depth It is important to know the exact penetration depth and concentration of oxygen for the understanding of microbial processes at the oxic/anoxic interface in sediments. Before Revsbech et al. (1980) introduced oxygen microelectrodes in ecological research, the oxic surface layer in sediments was assumed to be identical with the brown oxidized surface layer; i.e.
Figure 4. Schematic drawings of oxygen microelectrode tips. The four electrode types indicate 10 years (1980–1990) of evolution in the Revsbech-electrode design, i.e. from the simple cathode type to the Clark type with a guard cathode. Modified from Revsbech et al. (1983) and Revsbech (1989).
the layer having positive redox potentials. However, the use of oxygen microelectrodes has shown that oxygen penetration depth generally is less than 10% of the oxidized layer thickness (Revsbech & Jørgensen, 1986). The redox potential of the remainder (suboxic) layer is kept positive by occasional oxygen input and the presence of considerable amounts of oxidized iron and manganese compounds. The first cathode type of oxygen microelectrode with external Ag/AgCl reference electrode was developed around 1980 (Revsbech et al., 1980), since then a number of improvements and new developments of electrode design have been made (Figure 4). The cathode electrodes of Revsbech et al. (1980) were made of 0.1 mm platinum wire enclosed by a thin glass casing. The platinum tip was electrolytically etched in saturated KCN to a diameter of 1–4 µm and covered with a polystyrene membrane. The final diameter of the electrode tip was less than 10 µm. The cathode microelectrode was later improved by coating the platinum tip with gold before application of the
4 membrane in order to increase electrode stability and signal quality (Revsbech et al., 1983). A considerable improvement was the development of a combined microsensor that is a small version of the conventional Clark electrode (Revsbech & Ward, 1983). In this microsensor, the gold coated cathode is situated behind an electrically insulating membrane of silicone rubber which is extremely permeable to oxygen. The cathode is bathed in an electrolyte solution of 1 M KCl into which an Ag/AgCl reference electrode is immersed. Finally, the stability of the ‘Revsbech’ microelectrode was improved be inserting an internal guard cathode that removes all oxygen diffusing towards the sensor from the internal electrolyte (Revsbech, 1989). More recently, a new fiber-optic oxygen microsensor (microoptrode) was developed (Klimant et al., 1995). The microoptrode is made by immobilizing an oxygen-quenchable fluorophore at the tapered tip of an optical fiber with a 15–40 µm core diameter. An optoelectronic system is used to illuminate the fluorophore (blue) and to detect the fluorescent light (red) from the fiber tip. The intensity of fluorescent red light proportionally increases with decreasing oxygen concentration. In contrast to oxygen microelectrodes, the microoptrodes are relatively easy to make, do not consume oxygen and show no stirring dependence. The optrode principle has recently been used to develop planar optrodes (fluorophore coated PVC sheets) for measuring fine scale two-dimensional oxygen distributions in sediments (Glud et al., 1996). During measurements, the microelectrode (optrode) tip is introduced into the substratum by a micromanipulator at steps of 25–100 µm with a precision better than 10 µm (Revsbech & Jørgensen, 1986). For in situ measurements in oceanic environments, microelectrodes have been successfully mounted on benthic landers of various designs (Reimers, 1987; Gundersen & Jørgensen, 1990).
Oxic and anoxic diagenesis Organic matter diagenesis Organic matter is degraded (mineralized) in sediments by an array of aerobic and anaerobic microbial processes with a concurrent release of inorganic nutrients (Figure 5). The actual rates of decay depend primarily on organic matter quality (i.e. the content of protein, cellulose, lignin etc.), age (decomposition stage) and temperature (season) (Fenchel et al., 1998). The chemical composition of organic matter in mar-
ine environments can be generalized by the following formula: (CH2 O)x (NH3 )y (H3 PO4 )z , where x, y and z may vary strongly depending on the origin and age of the material. For marine organic matter (e.g. phytoplankton) having the Redfield composition: x = 106, y = 16, and z = 1. A number of organisms including bacteria, fungi and micro- and macrofauna are responsible for the aerobic degradation of organic carbon (Fenchel et al., 1998). Almost all of these have the enzymatic capacity to perform a total mineralization of organic substrates. Organic matter is, therefore, completely metabolized by a single organism to H2 O, CO2 and inorganic nutrients using oxygen as electron acceptor according to the following stoichiometry: (CH2 O)x (NH3 )y (H3 PO4 )z + xO2 → xCO2 + yNH3 + zH3 PO4 + xH2 O.
(1)
However, due to an efficient energy metabolism, a large fraction of the metabolized organic matter ends up as cell material. A unique feature of aerobic decomposition is the formation and consumption of reactive oxygen-containing radicals such as superoxide anion (·O2 − ), hydrogen peroxide (H2 O2 ) and hydroxyl radicals (·OH). These are capable of of breaking bonds and depolymerize relatively refractory organic compounds like lignin (Canfield, 1994). As the oxic (oxygen containing) zone in coastal sediments usually is limited to a thin uppermost layer, a large fraction of the organic matter is buried in a more or less decomposed form into anoxic layers. Here, anaerobic decomposition is accomplished by mutualistic consortia of bacteria because no single type of anaerobic bacterium seems capable of complete mineralization (Fenchel et al., 1998). Anaerobic decomposition occurs stepwise, involving several different functional types of bacteria (Figure 5). First, the large and normally complex polymeric organic molecules stepwise are split into water soluble monomers (amino acids, monosaccharides and fatty acids) by hydrolysis and fermentation under the production of energy and release of inorganic nutrients (Kristensen & Hansen, 1995), e.g. mixed propionate and acetate formation: 8(CH2 O)x (NH3 )y (H3 PO4 )z → xCH3 CH2 COOH + xCH3 COOH +3xCO2 + 3xH2 + yNH3 + zH3 PO4 .
(2)
The small organic acids are then oxidized completely to H2 O and CO2 by a number of respiring mi-
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Figure 5. The idealized vertical distribution of diagenetic processes in marine sediments. The oxic zone is illustrated by an oxygen profile (white zone), the suboxic zone is shown as the layer where the redox discontinuity is evident (light cross-hatched), the reduced zone is shown as the layer where Eh is below zero (dark cross-hatched). The depth scale is arbitrary.
croorganisms using a variety of inorganic compounds as electron acceptors. The individual anaerobic respiration processes generally occur in a sequence with depth in the sediment according to the availability of electron acceptors: Mn4+ NO3 − , Fe3+ , SO4 2− and CO2 respiration (Figure 5). The actual sequence is determined by the ability of each electron acceptor to receive electrons, and thus the energy output per degraded organic carbon atom (Fenchel et al., 1998), e.g. nitrate respiration (denitrification) is favored energetically compared to sulfate reduction. The suboxic zone contains the most potent anaerobic electron acceptors, Mn4+ , NO3 − and Fe3+ . The transition from one electron acceptor to the other downwards in the sediment occurs when the most favorable is exhausted. “When the best is gone, one has to accept something less good”. However, some vertical overlap may occur between the various zones. Only two examples of anaerobic degradation stoichiometries, denitrification and sulfate reduction, will be presented here: Denitrification :
CH3 COOH + 1.6NO− 3 +
1.6H+ → 2CO2 + 0.7N2 + 2.8H2O. Sulfate reduction : CH3 COOH 2CO2 + S2− + 2H2 O.
+ SO2− 4
(3) → (4)
The strict vertical distribution of electron acceptors as depicted in Figure 5 is an over-simplification of the true spatial distribution. The influence of sediment inhomogeneities, such as worm burrows, on porewater profiles and vertical distribution of microbial processes has been clearly documented (Aller, 1982). Furthermore, patches associated with e.g. fecal pellets are known to create anaerobic microniches, where anaerobic processes such as denitrification and sulfate reduction occur in otherwise oxic surface sediments (Jørgensen, 1977; Jahnke, 1985; Brandes & Devol, 1995). Nevertheless, the usually observed decreasing degradation rate with depth in sediments is not primarily caused by the less efficient electron acceptors in the deeper layers, but rather by the decreasing quality of organic matter (lability or degradability) with depth (Canfield, 1994). Even within a few mm thick oxic zone, the decreasing degradability may be evident as a considerable reduction in volume specific oxygen uptake with depth (Jensen et al., 1993; Figure 6). However, anaerobic bacteria appear more limited than aerobic organisms in their ability to depolymerize certain large complex molecules. These include among others saturated hydrocarbons (Schink, 1988), certain
6 Table 1. Importance of different carbon oxidation pathways in sediments from different depths in the Skagerrak. Rates are given in mmol m−2 d−1 . Numbers in brackets indicate the fraction (%) of total carbon oxidation by each pathway. From Canfield et al. (1993a)
190 m Respiration type Oxygen Nitrate Manganese Iron Sulfate
Figure 6. A sediment oxygen profile (full line) with estimated volume specific rates of oxygen consumption (dotted line). Oxygen consumption was estimated from changes in curvature of the oxygen profile. The oxygen consumption down to 2 mm is due to aerobic respiration, whereas the peak between 2 and 3 mm depth is caused be reoxidation of reduced inorganic metabolites. The horizontal line indicates the sediment–water interface. Modified from Jensen et al. (1993).
pigments (Sun et al., 1993a) and lignin (Benner et al., 1984). Separation of total benthic metabolism into respiration types Quantification of sediment respiration processes and separation of total benthic metabolism into individual processes is problematic. Only total metabolism (measured as total O2 or CO2 flux; Kristensen & Hansen, 1999), sulfate reduction (measured by 35 S assay; Fossing & Jørgensen, 1989) and nitrate respiration (measured by 15 N assay; Nielsen, 1992) can be determined directly on undisturbed sediment. The remainder, O2 , Mn4+ and Fe3+ respiration, has to be deduced indirectly from the shape of porewater profiles, from reaction rates in sediment incubation or by simple subtraction. By subtracting measured rates of sulfate reduction from measured rates of total sediment O2 uptake, oxygen respiration and sulfate reduction have generally been estimated to contribute by about 50% each to total benthic metabolism in coastal sediments (Jørgensen, 1983). In many organicrich sediments, however, sulfate reduction have been
2.1 (13.6) 0.5 (3.2) 0.0 (0.0) 5.1 (32.1) 8.1 (51.1)
Carbon oxidation 380 m 695 m
1.7 (17.4) 0.4 (3.6) 0.4 (3.8) 0.6 (5.7) 0.0 (0.0) 9.9 (90.7) 5.2 (50.9) 0.0 (0.0) 2.9 (27.9)
