Limnol. Oceanogr., 40(8), 1995, 1430-1437
0 1995, by the American
Society of Limnology
and Oceanography,
Inc.
Aerobic and anaerobic decomposition of organic m.atter in
marine sediment: Which is fastest?
Erik Kristensen
Institute of Biology,
Odense
University,
DK-5230
Odense
M, Denmark
Saiyed I. Ahmed and Allan H. Devol
School
of Oceanography,
Box 357940,
University
of Washington,
Seattle
98 195
Abstract
The enigma of aerobic vs. anaerobic decomposition in marine sediments was addressed by means of a
thin-layer incubation technique. Two different 14C-labeled plant materials, aged diatoms (Skeletonema costatum) and fresh barley hay, were each mixed into intertidal sediment and spread in a 1.5-mm layer on the
bottom of oxic and anoxic chambers. After a 27-d incubation, conditions in all chambers were switched
from aerobic to anaerobic and vice versa for 11 d. Rates of 14C0, evolution in diatom chambers showed
that aerobic carbon mineralization
was - 10 times faster than anaerobic both before and after the switch.
Low rates of [14C]DOC release suggested that the limiting step of an,aerobic decay was the initial hydrolytic
and fermentative enzymatic attack on the predecomposed diatoms. Initial carbon mineralization
of barley
hay was not affected by the presence or absence of oxygen. Leaching of DOC from the fresh barley hay
supplied anaerobic respirers with labile substrates. When leaching ceased and after the aerobic-anaerobic
switch, the rate of anaerobic mineralization
was reduced. Mineralizat:.on of leachable and easily hydrolyzable
compounds from fresh plant detritus is equally fast under aerobic ant! anaerobic conditions. When structural
components dominate the particulate remains, anaerobic processes are hampered by inefficient and slow
bacterial hydrolysis of structurally complex macromolecules.
In recent years, much effort has been devoted to determining whether microbial decomposition of organic
matter in marine sediments is faster under aerobic or
anaerobic conditions (e.g. Canfield 1994). However, the
results of various studies have pointed in quite different
directions. Aerobic oxidation has generally been accepted
to be an important decomposition process in undisturbed
marine sediments (e.g. Jorgensen 1983). Recent studies
have challenged this by arguing that most of the measured
oxygen flux into coastal sediments is used to oxidize reduced inorganic metabolites and not organic carbon (Canfield et al. 1993). Since organic particles are deposited
and degraded initially on the oxic sediment surface before
being buried into the anoxic layers, aerobic decomposers
are exposed to more labile substrates than are their anaerobic counterparts. Substrate lability usually decreases
rapidly with depth, even in moderately bioturbated coastal sediments (Henrichs and Reeburgh 1987; Kristensen
1993). A direct comparison between aerobic rates at the
sediment surface with anaerobic rates in subsurface layers
may therefore be deceptive. Nevertheless, many studies
comparing aerobic and anaerobic decomposition in slurry
and sediment incubations conclude that aerobic decomposition of a variety of organic substrates is faster (Benner
Acknowledgments
We thank Hanne Brandt for assisting with the analytical work.
E.K. was supported by grant 11-O 117- 1 from the Danish Natural Sciences Research Council. S.I.A. acknowledges ONR support.
1430
et al. 1984; Lee 1992) or slower (Sun et al. 1993b), while
others indicate that oxygen has no significant impact on
the rate of organic matter degradation (Kristensen and
Blackburn 1987; Lee 1992).
Aerobic heterotrophic microorganisms are known to
completely metabolize macromolecular carbon from organic particles to CO2 and cell biomass, whereas anaerobic decomposition is accomplished by mutualistic consortia of organisms. The initial steps of anaerobic decay
are the hydrolysis and fermentation of complex organic
structures t’o smaller moieties of low-molecular-weight
organic acids (e.g. acetate). Many of these compounds can
be directly mineralized to CO2 by microorganisms respiring with various oxidized inorganic compounds (e.g.
N03- and !504*-) as electron acceptors (Jorgensen and
Sorensen 1985). It is therefore important to realize that
differences in reaction rates between aerobic and anaerobic decomposition can occur at two levels: the initial
cleavage of particulate and other large macromolecules
and the fina: oxidation to inorganic mineralization products. Althot:gh studies have considered these two levels
(e.g. Henrichs and Reeburgh 1987; Canfield 1994), not
all differentiate between them in their interpretation of
organic matter decomposition.
Our purpose was to determine rate-limiting steps and
relative speed of aerobic and anaerobic decomposition
processes in marine surface sediments. We examined the
impact of molecular oxygen on the initial microbial attack
and the terminal oxidative mineralization of two 14Clabeled subsrates - aged diatom detritus and fresh barley
hay- by means of a thin-layer sediment incubation technique.
1431
Aerobic and anaerobic decay
Table 1. Elemental composition (C and N) and specificactivity of the 14C-labeledbarley hay and predecomposedSkeletonema costatum used in the decomposition experiment.
14
12
-
10
-
8
-
6
-
4
-
Materials and methods
2
-
Surface sediment (O-l-cm depth) and subsurface sediment (8-IO-cm depth) were collected from the intertidal
zone in False Bay, San Juan Island (48”30’N, 123”05’W),
Washington, in May 1994. The sediment was organicpoor (- 1% LOI) and well-sorted fine sand, with a medium grain size of 0.122+0.0 11 mm. Surface sediment
was oxidized with a brownish color down to -0.5-cm
depth; subsurface sediment was uniformly gray. There
was no smell of free hydrogen sulfide and no visible sign
of iron monosulfide in subsurface sediment. The sampled
sediment was stored cool (5°C) for - 5 d until further
handling in the laboratory.
Homogeneously 14C-labeledSkeletonema costatum was
harvested by continuous flow centrifugation
from
H14C0,--enriched cultures in the exponential growth
phase. After rinsing to remove excess H14C03-, the retained portion of labeled diatoms was mixed (1 :S) with
an unlabeled batch grown under similar conditions. Before use, the mixture was predecomposed aerobically in
a seawater slurry to half of the original activity (40 d, Fig.
1). The homogeneously 14C-labeled barley hay was grown
at the Ris~ Nuclear Power Testplant (Denmark) in a 14C02
atmosphere for - 1 month before being harvested and
dried (60°C). The dried material was ground, and the size
fraction < 500 pm was used. The elemental composition
and specific activity of both 14C-labeled mixtures are given in Table 1.
In order to not favor any depth related processes, we
mixed surface and subsurface sediment (1 : 1) 2 d before
the start of the experiment. The next day, the mixture
was split into two portions of 100-g wet wt each. To one
portion we added 4.4-g-ww 14C-labeled and predecomposed diatoms, S. costatum (denoted diatom sediment);
to the other portion we added 0.33-g-dw 14C-labeled barley hay (denoted hay sediment). After thorough mixing,
the labeled sediment was allowed to rest at 15°C overnight
before we transferred portions of 10-g ww to each of 12
incubation chambers (237-ml straight-sided glass jars,
7-cm i.d.), diatom sediment (27.2 kBq) in six chambers
and hay sediment (40.5 kBq) in another six chambers.
The added sediment was equivalent to a layer 1.5 mm
thick. After the chambers were filled with 28%0seawater,
they were sealed with rubber stoppers and, in series of
three, connected with 2-liter seawater reservoirs via 2-mmi.d. nylon tubing (Fig. 2).
Flow of water between each chamber and the reservoir
0
-
C content, mmol (g dw)-’
N content, mmol (g dw)-’
C : N ratio, molar
Sp act, kBq (mmol C)- 1
S. costatum
Barley hay
10.61
1.21
32.24
3.24
8.8
27
40
10.0
0
10
20
30
40
Days
Fig. 1. Ratesof total dissolved 14C(TC) loss from the Skeletonema costatum slurry during predecomposition.
was maintained with a peristaltic pump at a rate of -3
ml min-l (chamber turnover time, 80 min). Hanging
magnetic bars activated by an externally rotating central
magnet (60 rpm) stirred all chambers. We aerated two of
the four reservoirs (aerobic diatoms, D,, and aerobic hay,
H,) continuously with moist air to maintain 100% oxygen
saturation, whereas the other two (anaerobic diatoms,
D,,, and anaerobic hay, H,,) received moist N2 to remove
oxygen. The gases were moistened (and N, equilibrated
with CO,) by bubbling through a 20-cm column of seawater. Frequent tests from the anaerobic reservoirs assured us that oxygen was always absent (standard Winkler
technique) and that total CO2 (TC02) and pH remained
within a range of 1.8-2.0 mM and 7.8-8.1, respectively
(TC02 determined by potentiometric Gran titration according to Talling 1973). Gases leaving both the aerobic
and anaerobic reservoirs were stripped of all CO, in a
series of two NaOH traps (200 ml, 0.5 M). Tests showed
that ~95% of the 14C02 entering each trap was retained,
so the combined efficiency of the two traps was ~99%.
Reservoirs and traps were renewed every third day. Water
samples taken from reservoirs at the start and end of each
3-d period were analyzed for dissolved inorganic nitrogen
(DIN = NH4+ + NO,- + N03-) by standard autoanalyzer techniques (Armstrong et al. 1967; Solorzano 1969).
The entire setup was kept in darkness at 15°C throughout
the 38-d experiment. From day 27 to the end, we switched
the gases(i.e. D,, and H,, reservoirs were aerated and D,
and H, reservoirs received N2).
The release of 14C-labeledsolutes ( 14C02and [ 14C]DOC)
from the sediment was determined on a 3-d basis with
samples taken from the reservoirs and traps after every
renewal. The flux rates obtained from each system represent the accumulated amount of dissolved 14Creleased
from three chambers. A volume of 75 ~1of 0.5 M NaOH
was added to 3 ml of filtered seawater from the reservoirs
and mixed with 15 ml of EcoLume (ICN Biomedicals)
scintillation cocktail in 20-ml scintillation vials. These
1432
Kristensen et al.
Table 2. Particulate organic C (POC)
in the sediment before and immediately
hay and Skeletonema costatum detritus
38-d incubation period. Values are given
determinations
[hmol (g dw)- ‘1.
0
S. costatum
Barley hay
158+19
266+8
175+23
199f20
158+ 19
286+ 12
18Ok23
175+17
PON
Before addition
After addition
Aerobic -end
Anaerobils - end
17+4
29kl
21+1
21+1
17-t4
32f 1
1822
17+1
C:N
Before addition
After addition
Aerobic - end
Anaerobic-end
9.OkO.9
9.3kO.O
8.4f0.8
9.5f0.7
POC
Before addition
After addition
Aerobic--end
Anaerobic-end
Chambers
Reservoir
Traps
Fig. 2. Schematic presentation of one of the four identical
incubation systems used in the experiment. Water flow (indicated by arrows) between incubation chambers and the seawater
reservoir is driven by a peristaltic pump, P. Flow of moistened
atmospheric air (aerobic incubation) and N, (anaerobic incubation) is bubbled through the reservoir and subsequently through
the two NaOH traps (direction indicated by arrows).
samples were counted for total labeled carbon ([14C]TC)
in a Packard 2200 CA Tricarb liquid scintillation analyzer
with internal quench correction. Then, 150 ~1 of 0.5 M
HCl was added to another 3 ml from the reservoirs and
shaken frequently for 2 d to release 14C0, before we added
scintillation cocktail and counted for [r4C]DOC. Trap
samples were treated like the [14C]TC samples from the
reservoirs except that no NaOH was added. We calculated
the total release of 14C0, from the chambers as the sum
of 14C0, activity in the reservoirs (i.e. the difference,
[14C]TC - [14C]DOC) and traps.
Samples of sediment for determination of particulate
organic carbon (POC) and nitrogen (PON) were taken
from both the initial mixtures and from each chamber at
the end of the experiment. A Carlo Erba EA 1108 elemental analyzer was used to analyze POC and PON content. 14C-labeled POC from the sediment was recovered
by trapping the evolved 14C0, from the effluent gas after
combustion in the CHN analyzer, using two 5-ml NaOH
(0.5 M) traps, and counting as described above. Tests
showed no cross-contamination between samples.
Results
The organic additions increased the POC and PON
content by 68 and 7 1%, in the diatom sediment and by
8 1 and 88%, in the hay sediment (Table 2). Decay processes(and leaching) throughout the entire 38-d experimental period reduced the POC enrichments by 62-87%.
This is equivalent to a mean POC removal rate [pmol C
(g ww)-l d-‘1 of 1.84 in D,, 2.16 in H,, 1.37 in D,,, and
2.26 in H,, chambers (Fig. 3). By relating the 38-d cumulative production of dissolved 14Cin the chambers to
the specific activity of the added substrates, the estimated
and N (PON) content
after additon of barley
and at the end of the
as mean k SD of three
9.0f0.9
9.OkO.2
9.7kO.3
10.2kO.7
contribution of these materials to the total removal of
carbon from the sediments is 96% in D,, 63% in H,, 64%
in Dan, and 69% in H,, chambers. Except for D,, where
almost all #ofthe POC loss is accounted for by the added
material, about a third of the POC loss originated from
the indigenous organic pool in the sediment. Accordingly,
the mean d.egradability of carbon from the added diatom
detritus was 34 times higher in aerobic and 3 times higher
in the anaerobic treatments compared to the indigenous
organic carbon in the sediment. Carbon in aerobic and
anaerobic hay detritus was degraded 2 and 3 .times faster,
respectively, than the indigenous sediment pool.
The rates of 14COZevolution in diatom sediments clearly indicated that aerobic mineralization of labeled carbon
was faster than anaerobic mineralization (Figs. 3,4). During the first 27 d (before the aerobic-anaerobic switch),
the D, chambers produced on average 8.7 (range 2.618.2) times more 14C0, than the D,, chambers. The influence of oxygen on microbial decay of predecomposed
diatom detritus is substantiated by the almost instant
change in sediment 14COZproduction after the aerobicanaerobic switch. The production of 14C02 in D,, chambers 3 d after the switch was similar to that observed in
the D, chambers before the switch, whereas the rates in
D, were close to the preswitch D,, level; the average postswitch ratio between D,, and D, chambers was 15.1 (range
2.4-30.7 1). Significant [14C]DOC evolution was only detected during the first 10 d in D, chambers, with 5.0-12.7
times higher rates than in D,, chambers. During the remaining pm- and postswitch periods, [14C]DOC production was generally low and only slightly higher in D,
compared with D,, chambers. The recovery of label from
the experimental chambers at the end (day 38) was 93%
in D, and 86% in D,, (Table 3). Of the initially added
label, - 16 and 47% remained as [14C]POC in D, and D,,
chambers, respectively, at day 38. It is important, how-
Aerobic and anaerobic decay
Diatom
A chambers
AN chambers
---- -
20
10
0
40
30
Days
Days
Fig. 3. Release rams of total dissolved C (TDC) (labeled + unlabeled) from diatom- and hay-amended sediment in aerobic and
anaerobic chambers during the 38-d incubation period. Connected symbols represent the dissolved C loss originating from the
added labeled materials, estimated from the measured 14C loss and the specific activity of the source materials. Aerobic rates-O;
anaerobic rates-O. Broken lines represent the mean loss rate of particulate organic C (POC) from sediment in aerobic (A) and
anaerobic (AN) chambers. Arrows indicate time of aerobic-anaerobic
switch.
100
100
J
I
: Diatom
Hay
80
Cl aerobic
4 anaerobic
switch
60
40
20
i
0
-1
30
'1 0
40
0
140
140
120
120
100
100
10
20
30
40
Hay
80
60
60
20
0
10
20
Days
30
40
0
10
20
30
40
Days
Fig. 4. Weight-specific rates of 14C0, and [14C]DOC release from diatom- and hay-amended sediment in aerobic and anaerobic chambers during the 38-d incubation period. Dotted
lines indicate the time of aerobic-anaerobic
switch.
1434
Kristensen et al.
Table 3. Budget of 14C in chambers with Skeletonema c:ostatum-amended sediment and
chambers with barley hay-amended sediment. Values are given as total activity in kBq for all
three chambers in each treatment. Initial values represent the added labeled particulate organic
C (POC). The day-27 values are the cumulative recovery of label in dissolved form during
the preswitch period. Final values represent the label recovered in various pools after 38 d.
Numbers given in parentheses are percentages of the initial addition. Recovery is the sum of
all final values.
S. costatum
Initial POC
Final POC
Day-27 DOC
Final DOC
Barley hay
Aerobic
Anaerobic
Aero bit
Anaerobic
81.4(100)
13.3(16)
81.4(100)
38.5(47)
121.5(100)
35.6(29)
121.5(100)
37.9(3 1)
8.9( 11)
9.1(11)
2.8(3)
4.5(6)
22.8(19)
26.0(2 1)
39.7(33)
41.8(34)
Day-27 CO,
Final CO,
50.7(62)
53.6(66)
8.5(10)
27.3(34)
45.3(37)
48.5(40)
38.8(32)
46.1(38)
Recovery
76.0(93)
70.2(86)
110.1(91)
125.8(104)
ever, to recognize that these figures include both the preand postswitch periods. Accordingly, the cumulative release of dissolved r4C-labeled compounds (14COZ +
[14C]DOC) at day 27 (the time of switching) accounted
for 73% in D, chambers and 13% in D,, chambers of the
added activity, which means that only 4% was released
in D, chambers from day 27 to 38 in contrast to 27% in
D,, chambers (Table 3).
The diflerence in decay rates and patterns between aerobic and anaerobic treatments in the hay-amended sediment was not as conspicuous as it was in the diatom
sediment. Carbon mineralization, determined as 14C02
production, before the aerobic-anaerobic switch was only
higher in H, than in H,, chambers during the first 10 d
(by a factor of 1.1-2.9). However, the difference was counterbalanced by a 2.1-3.2 times higher [ 14C]DOC production in the anaerobic chambers during the same period
(Fig. 4). In both H, and H,, chambers, carbon mineralization rates declined rapidly after day 10, reaching a
constant level around day 20. The decreasing mineralization activity was associated with a similar rapid decline
in [ 14C]DOC production from day 10 to day 20. Recovery
of label from the experimental chambers at the end (day
38) was 9 1% in H, and 104% in H,, (Table 3). About 29
and 3 1% of the initially added activity remained as
[14C]POC in H, and H,, chambers, respectively, at day
38. The cumulative release of dissolved 14C-labeled compounds ( 14COZ+ [ 14C]DOC) at day 27 (the time of switching) accounted for 56% of the added activity in the H,
chambers and 65% in the H,, chambers (Table 3). This
means that only 5 and 7%, respectively, was released from
day 27 to 38.
No significant PON enrichment (O-6%) was evident in
the hay sediment (H, and H,,) after 38 d compared to
the initial indigenous pool. PON in the predecomposed
diatom material (D,, D,,) seemed less reactive, since a
24% enrichment
remained at the end. The loss of particulate N from the sediment was not reflected in the dissolved inorganic N (DIN) pools in any of the treatments.
On the contrary, both NH4+ and N03- actually decreased
in reservoirs during the last seven of the 3-d intersampling
periods (N II, + from about 5 to 2 PM in the aerobic and
5 to 1 PM in the anaerobic reservoirs; N03- from about
9 to 3 PM in the aerobic and 9 to 0 PM in the anaerobic
reservoirs), Because no measurements of DIN changes in
reservoirs were made during the first 15 d, when most of
the nitrogen loss probably occurred (Otsuki and Hanya
19723), the DIN values should be viewed with caution.
In any case, nitrogen seemed to be lost from both aerobic
and anaerobic chambers.
Discussion
The thin-layer approach used in this experiment, where
a 1.5-mm sediment layer was spread on the bottom of
the incubation chamber, assured that all sediment particles in the aerobic treatments were in contact with free
O2 at any time when the overlying water was kept at full
air saturation. Oxygen usually penetrates at least 1.5 mm
into organ&poor, sandy marine sediments underlying
oxygenated water (Revsbech and Jorgensen 1986). A similar thin-lay,er technique with redox oscillations for use
in decomposition studies has been presented recently (Sun
et al. 19933; Aller 1994). Compared to classic slurry incubation techniques, the thin-layer approach results in a
minimum of physical disturbance, allowing an assessment of microbial processes in surficial sediments under
natural diffusion-limited conditions (Jorgensen 1978; Sun
et al. 1993a ). As the initial sediment handling (sampling,
homogenization, and storage) may have temporarily affected both aerobic and anaerobic bacterial communities
in the sediment, our results are not expected to be equivalent to in situ rates. However, the comparative aspect
of this laboratory experiment dealing with aerobic vs.
anaerobic p:rocessesis considered representative of natural surface sediments.
All leachable and easily hydrolyzable materials (the
reactive G, fraction, sensu Westrich and Berner 1984)
from the diatoms added to D, and D,, chambers were
probably released as DOC and mineralized during the
Aerobic and anaerobic decay
40-d predecomposition period (Fig. l), as indicated by
the high initial decay rate and subsequent rapid decline
in the diatom slurry. In a similar slurry experiment with
fresh microalgae (Scenedesmus sp.), Otsuki and Hanya
( 1972a, b) found DOC and CO2 release to be rapid during
the first 20-30 d of decomposition.
The generally low levels of [14C]DOC found in the D,,
chambers (Fig. 4) suggest that the limiting step of anaerobic decay of the predecomposed diatoms was the initial
hydrolytic and fermentative enzymatic attack on the more
complex and polymeric particulate remains-terminal
carbon mineralization by sulfate reducers respired DOC
as fast as it was produced. Kristensen and Hansen (1995)
also observed that after 1 month of anoxic incubation,
sulfate reduction became limited by DOC availability in
coastal sediments amended with yeast and seagrass detritus. Because sediments receive organic matter mostly
in a particulate form, which is structurally too large to be
readily transported inside bacterial cells, the rate-limiting
step in mineralization of organic matter must be extracellular enzyme-associated hydrolysis of macromolecules
(Ahmed et al. 1992).
Aerobic decomposition involves innumerable enzymes, many of which are specific to individual classes
of compounds, and each compound is usually rapidly and
completely metabolized by a single microorganism (Canfield 1994). Anaerobic respirers (e.g. sulfate-reducing and
methanogenic bacteria) on the other hand, which are unable to degrade most polymeric organic compounds (Jsrgensen and Bak 199 1; Ahmed et al. 1992), may rely on
relatively slow hydrolytic and fermentative bacteria for
the supply of metabolizable low-molecular substrates. Although Westrich and Berner (1984) also observed that
aerobic mineralization of planktonic material was 2-3
times faster than anaerobic, they reasoned that the differences were largely illusory due to different mixing rates
in the two systems and possible geopolymerization in the
oxic system. In agreement with our study, however, F.
0. Andersen (pers. comm.) found that decomposition of
the more reactive G2 fraction from S. costatum after 2030 d in sediment was 5 times faster under aerobic than
under anaerobic conditions. Furthermore, he found only
limited impact of oxygen on the overall decomposition
rate of the leachable and easily hydrolyzable (G,) fraction.
It is evident, therefore, that organic components (e.g.
carbohydrates, proteins, lipids, pigments) of different
structural complexity are decomposed at different rates
in sediments (Henrichs and Doyle 1986; Hedges et al.
1988; Sun et al. 19933) and that aerobic and anaerobic
conditions may affect the hydrolysis and mineralization
processes of each component differently. Accordingly,
Harvey et al. ( 1986) found that bacterial membrane lipids
are degraded twice as fast under aerobic than anaerobic
conditions. Lee (1992) reported that mineralization of
diverse types of small biogenic monomers generally was
faster under aerobic than under anaerobic conditions, although in some cases,rates were equal or lower in aerobic
systems. Recently, Sun et al. (1993a) showed that degradation of bulk sedimentary chlorophyll a is - 3 times
faster during aero bit than anaerobic incubations.
1435
In contrast, several studies have indicated that rates of
aerobic and anaerobic decomposition of fresh microalgal
material are similar (Foree and McCarty 1970; Jewel1and
McCarty 197 1; Otsuki and Hanya 1972a, b). In their
closed freshwater slurries, however, Otsuki and Hanya
( 1972a, b) found that aerobic mineralization was - 3 times
faster than anaerobic mineralization. The correspondingly high accumulation of DOC in the anaerobic slurries of
these studies was caused by rapid initial leaching of DOC,
which was inaccessible for the anaerobic respirers, i.e.
methanogens. In accordance with our open-system experiment, no further DOC accumulation was observed in
the closed-system batch experiment of Otsuki and Hanya
(1972a, b) after -40 d of incubation.
Aerobic respirers seem to respond rapidly to the extensive leaching of DOC from the fresh barley hay detritus, as indicated by the high initial 14C02 production
and relatively low net [14C]DOC production. The anaerobic respirers, on the other hand, suffered through a lag
phase of a few days before the capacity of the population
was at its maximum. However, after reaching this stage,
the anaerobes could keep pace with the aerobes during
the remaining preswitch period. Both F. 0. Andersen
(pers. comm.) and Kristensen and Hansen (1995) attribute a similar initial lag phase of sulfate reduction in sediments with high concentrations of DOC to the time needed for the sulfate reducers to reach their optimum population size and maximum enzyme activity. The decreasing mineralization of DOC in both H, and H,, chambers
represented the gradual exhaustion of the reactive G, fraction of the hay detritus. Bacterial hydrolysis of POC to
DOC and mineralization of DOC to CO2 appeared to be
in a dynamic balance after day 20; the overall rates were
apparently limited by the former process. Most of the
carbon being degraded during the first 27 d probably originated from labile cellulose and xylose, since these two
components account for 60% of dry barley hay (Chesson
et al. 1983).
The rapid decline in carbon mineralization in both H,
and H,, chambers after the aerobic-anaerobic switch at
day 27 was associated with a reduced initial hydrolytic
attack on POC because there was no simultaneous increase in net [14C]DOC production. The new redox conditions probably caused instant inhibition or death of
most microbial cellulose decomposers. Subsequently, carbon mineralization in the postswitch aerobic H,, chambers increased gradually, reaching a level similar to the
preswitch activity at the end (day 38). No such increase
was evident in the anaerobic H, chambers. The low and
constant postswitch rates in the anaerobic chambers indicated that the organic substrates remaining in the barley
hay detritus were relatively refractory and energetically
unfavorable for growth and establishment of new anaerobic microbial communities. Lignin, a common structural component of vascular plants rich in slowly degradable aromatic ring units, is probably the major constituent of the barley hay detritus remaining at day 38,
since it accounts for >20% of the dry weight in fresh
barley hay (Chesson et al. 1983). Benner et al. (1984)
found that the anaerobic decomposition rates of ligno-
1436
Kristensen et al.
cellulose and lignin are only l-10% of the aerobic rates;
this may explain the final low activity in the postswitch
anaerobic barley hay sediments.
For an understanding of the differences between aerobic
and anaerobic degradation processes, it is necessary to
recognize the function of molecular oxygen under aerobic
conditions. Oxygen serves two different functions in the
degradation of organic matter: that of a terminal electron
acceptor for electrons released during oxidation of organic
carbon and that of a reactant in the oxygenase catalyzed
primary attack on the substrate molecules. Whereas the
first function may be transferred in the absence of oxygen
to other oxidized compounds, such as sulfate, there is no
equivalent to oxygen that can fulfill its functions as a
reactant in the primary transformation of important substrates. Of the long list of primary reaction types observed
in natural environments (Menzie 1980), only a few can
be catalyzed in the absence of oxygen. Because there are
limitations to the ability of anaerobic bacteria to hydrolyze certain classes of structurally complex and aromatic
organic compounds, the slower rates of decomposition in
the anoxic zones of most sediments can be explained by
the fact that organic matter, having already been partially
decomposed before burial in anoxic sediment, generally
is less labile than the organic matter at the sediment surface (Canfield 1994). The key to understanding the difference between aerobic and anaerobic decomposition is,
therefore, the nature of the organic substrate, i.e. its origin
and age (stage of decomposition). Fresh, readily degradable organic material is degraded at similar rates in the
presence and absence of oxygen, whereas old and refractory materials resist anaerobic decomposition. The overall differences in the ability of aerobes and anaerobes to
degrade certain classes of sedimentary organic material
may affect carbon burial and preservation in sediments.
Enhanced carbon preservation can be explained if more
refractory carbon is less efficiently decomposed in the
absence of oxygen (Canfield 1994).
The answer to the question raised here, “which is faster,
aerobic or anaerobic decomposition?,” is not obvious,
but our results suggest that the rate of decay under different redox conditions depends primarily on the age and
origin and thus the chemical composition of the organic
matter under consideration. The terminal oxidation rate
of simple and low-molecular-weight dissolved organic
molecules originating from the initial leaching and early
hydrolysis of fresh plant detritus is similar, with both
oxygen and other oxidized compounds (e.g. sulfate) as
electron acceptor. When structural components (e.g. lignin and complex lipids) become a dominant fraction of
the particulate remains in sediments, anaerobic processes
are gradually hampered by the inefficient and slow bacterial hydrolysis of the structurally complex and aromatic
macromolecules.
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Submitted: 13 January 1995
Accepted: 3 May I995
Amended: 7 August 1995