Differential Contribution of Bacteria to Sedimentary Organic Matter In Oxic and Anoxic Environments,...

~ Pergamon Org. Geochem. Vol. 26, No. 9/10. pp. 545-563, 1997

© 1997 Elsevier Science Ltd. All rights reserved Printed in Great Britain

PII: S014f~i380(97)00018-1 0146-6380/97 $17.00 + 0.00

Differential contribution of bacteria to sedimentary organic matter in oxic and anoxic environments, Santa Monica Basin, California

C H A N G R U I G O N G and D A V I D J. H O L L A N D E R

Department of Geological Sciences, Northwestern University, 1847 Sheridan Road, Evanston, 1L 60201, U.S.A.

Abstract--Two sediment box-cores in the Santa Monica Basin (SMB), one from the depocenter (900 m water depth) with anoxic bottom water and one from the periphery (840 m water depth) with oxic bottom water, were comparatively studied to assess the role of bottom water oxygen conditions to organic matter preservation and the differential contribution of bacteria to sedimentary organic matter accumulation and composition. Fatty acids from the sediment extracts were analyzed for their abundance and carbon isotopic compositions. Molecular and isotopic evidence indicates that most of the short-chain FAs from the SMB sediment extracts are sourced by bacteria as a result of intense microbial recycling and resyntheses of organic matter, especially in the aerobic environment at the periphery site. Long- chain fatty acids are probably derived from terrestrial sources and partially sourced by microbial processes. Very depleted 6t3C values (-30 to -45%0) of bishomohopanoic acids and triglycerides suggest the presence of chemoautotrophic bacteria in the anoxic water column and in the sediments. There is a much greater contribution from anaerobic microbial biomass and chemoautotrophic bacteria in the depocenter sediments relative to the periphery sediments. In addition, organic matter exhibits bulk and molecular characteristics of enhanced preservation under the condition of anaerobic decomposition at the depocenter site, especially at the sediment/water interface and the first couple of centimeters. Together, enhanced preservation with the addition of microbial biomass could explain the higher organic accumulation rates and H/C ratios in the basin depocenter and the periphery sediments and the trend of decreasing 6i3c values of bulk organic matter in the depocenter sediments. This study has im- plications for understanding the role of anoxia and associated bacterial processes in controlling the geochemical characteristics ancient organic carbon-rich sediments deposited under oxic and anoxic conditions. © 1997 Elsevier Science Ltd

Key words--fatty acids, isotopes, aerobic/anaerobic bacteria, oxic/anoxic sediments, chemoautotrophy, organic matter preservation, Santa Monica Basin, California

INTRODUCTION

The Santa Monica Basin, one of the several rift basins off the coast of California (Fig. 1), is situated within the Southern California Countercurrent, a seasonal poleward flow that forms a large-scale eddy in the California Current (Jackson et al., 1989). In the basin depocenter, bot tom water oxygen contents are at or below 0.1 ml 1 - l so that bioturbation is inhibited, thus preserving the primary sedimentary structure of finely laminated sediments with high organic carbon contents. Anoxic bot tom water conditions first appeared about 350 yr before the present and were restricted to the northeastern basin floor sector at 900 m. Over the past 350 yr the anoxic bot tom water mass has expanded to cover most of the basin floor below depths of about 850 m. Weaker oceanic circulation after the little ice age, and increased nutrient input due to land use change and human populat ion growth in the nearby Los Angeles area, caused the expansion of anoxic bot tom water (Gorsline, 1992). Finely-laminated sediments range in thickness from about 25 cm in the oldest northeastern region of the basin down to

0 cm at the edge of the non-bioturbated zone where the anoxic/oxic interface is now located (Fig. 2).

A bulk organic geochemical study (Hollander et al., 1994) has compared two sediment cores, one from the basin depocenter at 900 m water depth and one from the periphery of the basin floor at 840 m water depth, and has assessed the role of bottom water oxygenation in controlling the organic matter accumulation and composit ion in the sediments. Because these two coring sites are very close to each other (15 km apart), similar bot tom water circulation, sedimentation processes, and settling flux of organic matter from the water column above have prevailed during the deposition of sediments for these two locations. The difference between the depocenter and the periphery settings is the availability of bot tom water oxygen, which must be responsible for the difference of organic matter quality and quantity between the two cores after the start of the basin anoxia. Prior to the onset of basin anoxia, both sites had similar organic carbon accumulation rates of about 0.5 mg C/cm2/yr. As the eutrophication of the basin increased and anaerobic conditions prevailed in the depocenter,

545

546 Changrui Gong and David J. Hollander

34 °

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Fig. 1. The location of the Santa Monica Basin (modified from Christensen et al., 1994).

34 °

33 °

TOC accumulation rate increased to a maximum of 1.45 mgC/cm2/yr, whereas at the periphery site under oxic bottom water condition TOC accumulation rate only increased to 1.1 mgC/cm2/yr (Fig. 3a). The H/C ratio of organic matter from the basin depocenter shows an increasing trend from

0.8 in 1450 AD to 1.4 in 1970 AD, and then for the most recent period decreases from 1.4 to 1.2, while for the basin periphery the H/C remains more or less constant up to the year 1900 and then it shows a sharp increase from 0.7 to 1.1 (Fig. 3b). Even though both sites had experienced increasing

119040 ' 119020 ' 119000 ' 118040 ' 1 8020 '

Sanla Barbara I ~ , , ~ I i

,,,[ ~ I ~ ~ " ~ ' " - " ~ Santa 3 4 ° 4 0 ' ~ ' J ' ~ ~_,, ~ [ ' ~ ' ~ o n i c a

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Fig. 2. lsopach map of laminated sediments in the Santa Monica Basin. The solid lines are basin bathy- merry in meters and the dashed lines indicate the thickness of laminated sediments in millimeters. Line of zero millimeter thickness marks the boundary of oxic and anoxic bottom waters. Point 1 and point 2 in circles are the locations of the two sediment cores described in this paper. Water depth at site 1 is

about 900 m and at site 2, about 840 m.

Contribution of bacteria to sedimentary organic matter

i

2000

1950

1900

1850

1800

1750

1700

1650

1600

1550

1500

1450 0.25 0.5 0.75 I 1.25

Organic carbon accumulation rate (mg C/cm2/yr)

Periphery < ~ ~ s e d ~

Depocelter ts

1.5 0.60

J i

0.80

H/C

)

~ r y sediments

4 I

1.00 1.20

ratio of organic matter

1.40

Fig. 3. Bulk characteristics of organic matter from the depocenter and the periphery sediments. The onset of lamination in the depocenter was at about 1550.

547

organic matter accumulation probably as a result of surface water eutrophication, it was noted that up to 50% of the increase in organic carbon accumulation rates and 80% of the increase in H/C elemental ratios in the depocenter, relative to the periphery, are related to the development and expansion of bottom water anoxia. The question that remains from that study is what process contributes to the enhanced organic matter accumulation and higher H / C ratios observed in the anoxic depocenter sediments. Is this a simple result of preservation due to different decomposition rates at different bottom water oxygen conditions? Can bacterial processes play a significant role in the differential organic matter accumulation at these two sites? If so, does bacterial biomass contribute selec- tively to the sedimentary carbon reservoir depend- ing on the chemical conditions in the water and sediments?

Bacteria occur in all present-day sedimentary environments. They have been identified in Antarctic sediments, deep-sea sediments, anoxic basin sediments, intertidal sediments, salt-marshes, mangrove sediments, lacustrine sediments, and elsewhere (Rowe and Demings, 1985; Alongi, 1987; Capone and Kiene, 1988). Bacterial populations as high as 5x l0 II cells g -l have been reported in some sediments (Alongi, 1989), corresponding to a bacterial biomass possibly as high as 1% of the dry weight of the sediment, thus a contribution to sedimentary TOC of possibly up to 50%. Bacterial numbers are generally highest at the sediment-water interface and show a marked decline with depth, due to a depletion of organic substrates on which the microbes can grow (Dale, 1974). However, recent investi-

gations have revealed subsurface maxima of bacterial activity in sediments at a depth of > 200 m by Parkes et al. (1997) and in excess of 500 m in the Japan Sea (ODP hole 798B) (Cragg et al., 1992). They suggested that bacterial distributions seem to be controlled by the availability of terminal electron acceptors, the bioavailability of organic matter, and biological and geothermal methane production at this site. Animal grazing, physical disturbance of the sediment, and timing and quality of the organic matter supply to the seafloor (Morrison and White, 1980; Kemp, 1987; Lochte and Turley, 1988; Miller, 1989; Demings and Baross, 1993) are also important determinants of bacterial abundance in marine sediments.

Various direct (plate counts, colony forming units, and most probable number) and indirect methods (the extraction of ATP and RNA) have been used for the measurement of microbial biomass (Craven et al., 1986; Craven and Jahnke, 1992; Getliff et al., 1992; Hurst et al., 1997). Fatty acids (FAs) of bacterial origin have been used extensively to assess the contribution of microbial biomass to the sedimentary organic matter (Cranwell, 1984; Gillan and Sandstrom, 1985; Hedrick et al., 1992; White, 1993). For example, iso- and anteiso-FAs, and hopanoid FAs were observed in the sedimentary environment and are believed to be bacterial contributions (Boon et al., 1977; Ourisson et al., 1984; de Leeuw et al., 1995). Here we present a combination of FA quantification and their carbon isotopic composition analyses to study sourcing and decomposition of FAs and the role of bacterial processes in this sedimentary environment. A comparative study of two


cores, one from the depocenter with anoxic bottom water and one from the basin periphery with oxic bottom water, was conducted. The importance of preservation and the contribution of microbial processes to the differential accumulation and composition of organic matter in these two cores are evaluated.

MATERIALS AND METHODS

Samples of sediment were obtained in a series of cruises across the Santa Monica Basin from the depocenter and periphery of the basin (Fig. 2). Cores were split on board ship into subsamples for freeze-drying at 1.5 mm, 3 mm, 5 mm, or 10 mm intervals. Homogenized subsamples were measured for concentrations of carbonate carbon and organic carbon using a UIC carbon dioxide coulometer (Model 5012) equipped with total carbon apparatus (Model 5120) and acidification module (Model 5130).

Extraction of lipids

Extraction of sedimentary lipids follows the modified procedure developed by Wakeham and Pease (1992) at Skidaway Institute of Oceanography. Freeze-dried sediment samples were Soxhlet-extracted with 2:1 MeC12:MeOH for 24 h to obtain the total lipid extract (TLE). Extracts were then washed with 5% NaC1 solution and extracted NazSO4 was added to the TLE to remove any water. TLEs dried under a slow stream of N2 gas were saponified in 1 ml 0.5 N KOH/MeOH plus 3 ml extracted water solution at 100°C for 2h. Neutral fractions of TLE were obtained by extract- ing the saponified TLE with hexane three times. The remaining saponified TLE was acidified to pH 2 by adding 6 N extracted HC1 and extracted with hexane three times to obtain the acid fractions. The acid fractions were methylated in 500 #1 10% BF3/ MeOH solution at 100°C for 2 h. The methylated acid fractions were fractionated into different compound classes by separating them with silica gel ( l .3g of 100-150 mesh, deactivated silica gel in 6 mm ID column) column chromatography. Fatty acid methyl esters (FAMEs) were eluted in 10% ethyl acetate/hexane, ct/fl-OH FAMEs in methanol. This paper only presents the results of FAMEs frac- tion. Quantification of other fractions has indicated that hydroxyl FAs are minor components in these sediment extracts (less than 20% of the total FA abundance).

Gas chromatography-mass spectroscopy

Compound identification was performed at Indiana University using a Finnigan MAT TSQ 700 equipped with a Hewlett-Packard 5890 Series II GC-MS system with an HP-1 capillary column (50 m x 0.32 mm). On-column injection was used

and the injector temperature was tracking the oven temperature. Oven temperature program was 50°C initial temperature, 15°C/min to 200°C, and 3°C/ min to 320°C and final time of 30 min, and a 1 ml/ min He flow rate. The operating conditions of the mass spectrometer were 200 V accelerating voltage, 1500 multiplier, source temperature 170°C, and manifold temperature 70°C; the transfer line temperature was 320°C. The mass scan was from 50 to 600 with one scan every 0.8 s.

Gas chromatography quantification

FAME fractions were quantified using a Hewlett- Packard 5890 Series II plus Gas Chromatograph. Samples were eluted using an HP-I capillary column (50m×0.32mm) with on-column splitless injection and flame ionization detector. Oven temperature program was similar to that for GC-MS. Androstane was coinjected as the internal standard. Concentration of individual compounds was determined quantitatively assuming that concentration is proportional to chromatogram peak area, and its response factor is the same as the internal standard.

Gas chromatography-isotope ratio mass spectroscopy

Isotopic compositions of individual compounds were determined on a Fison ISOCHROM-GC (GC 8000 Series 8130) and VG Optima Mass Spectrometer instrument. The same type of GC column and similar temperature programs were used in the GC. The temperature at the interface was 350°C, the furnace 850°C, and cooling trap -100°C. The reference gas is calibrated against standards from the National Institute of Standard and Technology. Androstane is coinjected as the isotope standard. Duplicate or triplicate analyses were performed for each sample. The precision for carbon isotopic composition in this continuous flow system is _+0.2%0. The isotopic composition of the methyl group in BF3/MeOH was determined on irmGC- MS to be -46.3%0. The isotopic compositions of FAs were obtained based on the mass balance con- sideration of methyl group in FAMEs.

Carbon isotopic compositions of bulk organic matter in the sediment samples were determined on an ISOCHROM EA (Carlo-Erba NA 1500 Series 2 NCS) coupled with a VG Optima Mass Spectrometer. The combustion temperature was 1020°C. A two-meter packed column was used to separate C and N. Urea was used as the standard analyzed every tenth samples. Triplicate analyses were performed for each sediment sample.

RESULTS

The identified FAs in the sediment extracts include: straight-chain saturated FAg from C~2 to C30, straight chain monounsaturated FAs with even

Contribution of bacteria to sedimentary organic matter 549

carbon number from C i 6 to C 2 6 , branched saturated FAs for C~3, q s , q 6 , C~7~ and C18, branched unsaturated FA C~7, isoprenoid FAs q 6 and C~7, and C32 17fl,21fl(H),-bishomohopanoic acid. There is essentially no difference in the suite of FAs between the depocenter site and the periphery site (Figs 4, and 5).

For the sediments from the basin depocenter, a bimodal distribution is observed for all the straight chain saturated FAs (Fig. 4): q6:0 and Ct8:0 dominate the short-chain FAs and C24:0 and C 2 6 : 0

dominate the longer-chain portion. Odd-numbered Ct~:o and q7:0 dominate branched saturated FAs with small quantities of q3:0, q6:o and qs:0.

30

DEPOCENTER SEDIMENTS

20

10

0

30

20

10-

.-. 0

30

'~ 20-

<

0-3 mm

45-48 mm

1o H I ,02,05° I I I I I I I I I I I I I I I I I I I I I i I I I I I I I I I I I i

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30"

249-252 mm

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i i i I I I i 1 i i i i I i I i I i I I I i i I I i I | I I i i i I i i i I I

~ ~ ~ u ~ w w ~ ~ c 3 ~ u ~ ~ ~ . ~ ~ . ~ o ~o--

"~ [ "~ ~ ~ ~ ~ "a

Fig. 4. Relative FA content in percentage in the depocenter sediments from different depths. The sampling interval is 3 ram.


20

15-

10-

5-

0

20

PERIPHERY SEDIMENTS

5-10 mm

. . . . . . , , , , , , , , , , , , , , , , , , ,~ ! , , , , , , , 15

10

5

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~ 15

< lO

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80-90 mm

15

10

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0 20

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0

150-160 mm

~,~, ..~.~,~,.~,.!~,~..~,~..~,, .~,~,~o_~o~o~o~. , , , , , , , , , , ,

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~ , . . . . . . . . . , i , , , , , , , . . . . . i . , - - ~ - - ~ I I I I I I I I I I

0 0 ~ 0 0 ~ O r ~ r ~ O ~ 0 0 0 0 r ~ r x

Fig. 5. Relative FA content in percentage in the periphery sediments from different depths. The sampling interval is l0 mm but 5 m m towards the surface.


Unsaturated FAs are dominated by Ci6:l and Cis:l. For all the straight-chain or normal FAs, there is a strong even-over-odd carbon number preference in the distribution, especially for FA with carbon- chain lengths greater than 22. C~s:o FA contributes a progressively greater proportion to the total FAs with increasing depth (Fig. 4). The percentage of iso-, anteiso-FA, short-chain unsaturated FAs all decrease with depth. The long-chain FAs (C>22) comprise a similar percentage of total FAs at all depths.

In the periphery sediments, there is also a bimodal distribution for all the identified FAs, one centered at Cj6:0 and the other centered at C24:0 (Fig. 5). Iso- and anteiso- C15:0 and Cl7:0 dominate the branched FAs. CI6:l and Cls:l are the main unsaturated EAs. With increasing depth, C16:0 remains the dominant FA, accounting for up to 15 20% of the total EAs (Fig. 5). Long-chain FAs comprise a greater proportion of the total FAs in the periphery sediment than in the depocenter sediment, and there is also a slight increase of long- chain FA proportions with depth.

Because the sedimentation rates have been almost identical for the two sites, and have not varied throughout the studied intervals, concentrations of FAs normalized to organic carbon instead of accumulation rate of FAs are used in presentation of results. In the depocenter sediments, most FAs, especially iso- and anteiso-Cls:o and ClT:O (Fig. 6a), odd-numbered short-chain alkanoic FAs (Fig. 6c), Ci6:t and Cls:l (Fig. 6e), and Cl4:0, show a sharp decrease (several folds) in their concentrations for the first couple of centimeters, and maintain fairly constant contents further downcore. Others, especially Cl2:0, C18:0 (Fig. 6g), and long-chain alkanoic FAs (Fig. 6i) have rather constant concentrations at all depths except for C24:0. Total FA abundance (Fig. 6k) also decrease sharply from the sediment surface to 70 mm depth, and then vary little with increasing depth.

The sharp decrease in concentrations of FAs in the depocenter sediments is not observed in the periphery sediments. Except for a slight decrease in the surface sediments, concentrations of most FAs remain fairly constant throughout all depths (Fig. 6b,d,f,h,j), as does the total FA concentration (Fig. 61). Total FA concentrations and concentrations of most individual FAs are much higher in the depocenter sediments than corresponding FAs in the periphery sediments, especially near the sediment surface.

The isotopic compositions of individual FAs and total organic carbon are presented in Fig. 7. 6~3C values for bulk organic carbon are within a range of-21%o to -24%0 with rather consistent values for the periphery sediments (Fig. 7d), whereas the depocenter sediments exhibit a decreasing trend of up to 2%0 from a depth of 130 mm to the surface

(Fig. 7c). Most short-chain FAs (C < 21) from both the periphery and depocenter sediments have 613C values from -25 to -30%o (Fig. 7a-d). Anteiso-C15:o are more depleted in this group. C16:0 and Cl8:0 have most enriched values and unsaturated Cl6:lta 7 and C~8:1,,~7 are more depleted that their saturated counterparts except close to the surface for the depocenter sediments. 61SC values of long-chain FAs (C > 21) are generally more negative than those of short-chain FAs (Fig. 7e,f). In both sediment cores, their isotopic compositions become more negative with increasing chain length from C2z:0 to C30:0. Shifts toward more negative values with shal- lowing depth occur for sediments from both sites, but larger shifts are observed in the depocenter site. Bishomohopanoic acids have 6t3C values ranging from -30%o at 165 mm depth to -45%o close to the surface in the depocenter sediments (Fig. 7a), and their 613C values decrease from -34%o at 100 mm depth to -42%o at 15 mm depth in the periphery sediments (Fig. 7b). Comparatively, much larger variations in 613C values of most FAs with depth are observed for the depocenter sediments than the periphery sediments.

DISCUSSION

Sources o f FAs in the Santa Monica Basin sediments

Traditional source assignments of FAs have attributed short-chain even-numbered FAs from Cl2 to C20 including saturated and unsaturated, isoprenoid FAs, and long-chain alkenoic acids to phytoplanktonic and zooplanktonic source (Boon et al., 1977; Volkman et al., 1981, 1989, 1991; Nichols et al., 1989; Wakeham, 1995), iso-, anteiso-, odd-numbered FAs ranging C12-C2~, and hopanoic acids to bacterial sources (Leo and Parker, 1965; Cooper and Blumer, 1968; Kates and Wassef, 1970; Goldfine, 1972; Cranwell, 1973; Erwin, 1973; Perry et al., 1979; Harvey et al., 1984), and long-chain FAs (C > 21) to terrestrial sources (Cranwell, 1974). According to this scheme, the relative percentage of FAs from different sources can be calculated and plotted against the depth (Fig. 8a,b). In the depocenter sediments, bacterial FAs make up about 20- 30% of the total FAs, about 40% near the surface, and slightly above 10% near the bottom in the non-laminated sediments. Terrestrial sources of FAs comprise a similar percentage of the total FAs as do the bacterial sources. They also have similar variations with depth, but in contrast, the terrestrial sources decrease to 15% at the surface. Algal sources make up 40-70% of the total FAs and exhibit an increasing trend with depth.

For the periphery sediments, bacterial source contributions are fairly constant at 20% of the total FAs, and exhibit a slight decrease with depth (Fig. 8b). Terrestrial FAs have an increasing trend with depth from 20% to 40%. On the other hand,

552 C h a n g r u i G o n g a n d D a v i d J. H o l l a n d e r

DEPOCENTER SEDIMENTS FA concentration ( gg/g C)

0 50 100 150 0 50

PERIPHERY SEDIMENTS

0 0 i

50 50 .... :.~

100 100

150 "~c~200

200 250

300 250

350 300

_ _

50

100

150

~ 200

250

300

0 10 20 30 40 50 60

" .___.~, . . . . C 1 9 : 0

0 50 100 150 200

C 1 6 : 1 o ) 7

........ ¢ ....... C16 :1co9

. . . . o . . . . C18 :1c07

. . . . ~ , . _ - C18 :1co 9

FA concentration ( ~tg/g C)

100 I

b

150

200

0 10 20 30 40 50 60 0 . . . ~¢ i i i d

50 i 100

150

200

250

30O 0 50 100 150

O ~ J t J

5O

100

150

200

250

350

50

.-, 100

150 i~J 0

250 ? 3oo i

350 300

Fig . 6 ( a ) - ( f ) (Caption opposite page)


E

t -

DEPOCENTER SEDIMENTS FA concentration ( I.tg/g C)

0 100 200 300 400 500 600 0 ...x_ ._,_h -, ' -~ O--

50

100

150 ~ + C12:0

200 ~ ........ o ........ C14:0

250 "~-~-- "9 "'~ .... o .... C16:0

300 : ~,:ii""" . . . . /s--- C18:0

350

0 50 100 150

i 50

100

150

"~ 2 0 0 1 ~ ....... o ........ C_26:0

250 . . . . o . . . .

300

350 j ~ " - ' ~ .... C3°:°

ca, O

0 0

50

100

150

200

250

300

350

I000 2000 3000 I ~ - - ~ . . . -

----O--- Total FA

PERIPHERY SEDIMENTS FA concentration ( t.tg/g C)

0 100 200 300 400 500 600 0

h 5O

100 ~t o

150 ~ o

200

250

300

0

50

100

150

200

250

300

0 50 100 I

150

0

50

100

150

200

250

300

0 1000 2000 I I :

} 3000

1

Fig. 6. Comparison of FA concentrations in pg/g of organic carbon vs. depth profiles between the depocenter sediments and the periphery sediments. The total depth plotted is 350 mm for the depocenter sediments and 300 mm for the periphery sediments, but these depths are correlated according to their sedimentation age. Laminated sediments start at about 250 mm depth in the depocenter sedi-

ments.


algal sources make up about 40-55% and have a slightly decreasing trend with increasing depth. As mentioned before, there has been equivalent organic matter flux from water column at both these sites. Comparing the FA sourcing patterns from these two sites, it seems that algal FAs were better preserved in the depocenter site with anoxic bottom

water. The selective preservation of terrestrial long- chain FAs over the algal short-chain FAs in the oxic sediment could explain the increasing percentage of terrestrial FAs and the decreasing percentage of algal FAs with depth in the periphery sediments. The contribution of bacterial FAs is higher in the depocenter sediments after the onset

e-.

50

100

150

200

250

300 a

350 1

-45 0

50

100

150

200

250

300 C

350 '

DEPOCENTER SEDIMENTS ~13C of FAs (%o)

-45 -40 -35 -30 -25 -20

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300

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PERIPHERY SEDIMENTS ~13C of FAs (%o)

-45

° t 50

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100

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300

350

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. . . m . . .

-45 0

C2°:° 50

C22:o 100

C24:0 150

C26:o

C28: ° 200

C3o:o 250

300

-40 -35 -30 -25

:Zro ; / / : /

O

Fig. 7. Comparison of carbon isotopic composition of individual fatty acids vs. depth profiles betwen the depocenter sediments and the periphery sediments. 613C values of total organic matter are also

plotted.

-20


D E P O C E N T E R S E D I M E N T S

relative FA content (%) 10 20 30 40 50 60 70

0

50

100

150

200

250

300 -

350

80

• O':::.. '::=O

'. /

200

250

300

bacterial source

....... O ....... algal source

.... O---- terrestrial source

P E R I P H E R Y S E D I M E N T S

relative FA content (%) 10 20 30 40 50 60 70

0 I~:~bl ' o ~ ' ' "6~ o

0 . . . . . . . . . . . . Q...O ~""0 100 %0 ~g"

°--,o... ?......8 ~'"O

80

Fig. 8. Variation of FA concentrations from algal, bacterial and terrestrial sources according to traditional source assignment.

of bottom water anoxia (above 250mm in the depocenter and 210mm of age equivalent at the periphery site), and is much higher at the surface relative to the periphery sediments.

However, given the fact that both algae and bacteria contain major amounts of even-numbered nor-

mal acids, we should reconsider the validity of this traditional source assignment of FAs. Bacteria pro- duce a great diversity of FAs including normal,

straight-chain, monounsaturated, branched, c(- and fl-hydroxy and cyclopropane types (Lechevalier and Lechevalier, 1988 and references therein). Marine bacteria contain Cj6:l, Cl6:0 and C~8:0 as their major acids (Oliver and Colwell, 1973). Therefore, the traditional assignment of attributing even-numbered short chain FAs to an algal source is incom- plete, since they can also derive from bacterial biosynthesis. The experiments of Rhead et al. (1971, 1972) pointed to rapid degradation and resynthesis of FAs by bacteria in sediments. The result is a replacement of algal acids by bacterial acids in an early stage of burial. Cranwell (1984) recognized that, in anoxic sediment, the distributions of the shorter-chain homologous free n-alkanes, alkanols, and alkanoic acids result from microbial synthesis using material initially at the sediment surface, rather than partial preservation of the lipids of primary source organisms.

Long-chain FAs are not the exclusive product of plant biosynthesis. They are also common lipids of microbes (Ratledge and Wilkinson, 1988), though in very small quantity. Some mycobacteria have

been shown to synthesize FAs ranging in chain length from 14 to 32 carbon atoms (Schweizer, 1988), and the FA distribution is distinctly bimodal throughout a wide variety of conditions with peaks at Ci6 and C24, as in the SMB sediments. The common occurrence of these long-chain FAs in the sedimentary environments might be the result of their relative resistance to heterotrophic metabolism. Literature on microbial lipid metabolism has indicated that C~0 to C20 n-alkanes are the most easily utilized followed by iso-alkanes, alkenes, simple aro- matics and aryl-alyl hydrocarbons (Finnerty, 1988). Long-chain alkanes (C25 to C5o) appear to be poorly utilized as substrates. Long-chain FAs could also be a poorly utilized substrate by bacterial communities. Haddad et al. (1992) had observed 6-7 times slower degradation rates for long-chain FAs relative to short-chain FAs. Thus, these long-chain FAs accumulate, instead of being consumed and resynthesized, which increases their relative concentrations in the sediment. Gillan and Johns (1986) have also pointed out that the chain-length selectiv- ity of bacterial degradative processes is expected to result in a relative enrichment of long-chain acids in marine sediments when compared to short-chain substrates (i.e. <C18). Therefore, most of the FAs in the Santa Monica Basin sediments could possibly be sourced by bacterial resynthesis. Carbon isotopic compositions of these individual FAs can give us additional information about their sources.

Stable isotopic composition of a specific molecule depends on a number of factors, including the iso-


topic composition of the source carbon (the substrate), the limitation of the substrate, and the kin- etic fractionation of carbon isotopes associated with the metabolic and biosynthetic processes (Macko et al., 1987; Peterson and Fry, 1987; Fisher, 1990; Hayes, 1993). Lipids are commonly depleted in tSC relative to whole cells or other major compound classes. This fractionation arises during the formation of acetyl-CoA by pyruvate dehydrogenase and is localized at the carboxyl position in the acetyl-CoA product (DeNiro and Epstein, 1977; Monson and Hayes, 1982; Melzer and Schmidt, 1987).

Organic molecules coming from the same source generally have similar 613C values (Monson and Hayes, 1982; Rieley et al., 1991). For Escherichia coli, Monson and Hayes (1982) observed only small variations of their isotopic compositions (-10.8 to -13.8%o) among the FAs (C14:0, Cl6:0, etc.). Rieley et al. (1991) found that leaf-wax n-alkanes show a large inter-species 6~3C variation o f - 3 0 . 1 to -38.7%o, which may be the result of genetic differences in plant adaptation and physiology, while the differences in 613C between n-alkane homologues from a particular tree species were small (generally within 2c0. Large variations of biomarker compound isotopic compositions are considered to be the result of different biomarkers coming from different sources (Rieley et al., 1991; Collister et al., 1992: Kohnen et al., 1992; Sinninghe Damste et al., 1993; Collister et al., 1994a; Freeman et al., 1994; lshiwatari et al., 1994; Kenig et al., 1994). However, variations of up to 6%0 were observed between n-alkane homologues for the plants studied by Collister et al. (1994b), though the interspecies variations of lipid isotopic composition are even larger. Summons et al. (1994) also observed, unexpect- edly, up to 14%o difference between squalene and hopan-29-ol from methanotrophic bacteria. They also noted a progressive isotopic depletion as a result of positive fractionation factors throughout the hopanoid biosynthesis sequence. Therefore care must be taken when interpreting the isotopic composition of individual biomarker compounds solely in terms of their source contributions.

In the depocenter sediments, the 613C values for FAs of definite bacterial origin (C15:0, iso-Cts:o and anteiso-Cis:o) range from -27 to -33%0 (Fig. 7a,c). Similar variations and ranges in c513C values of Cl4:0, C17:0, and C20:o with those of bacterial FAs suggest that they are also of bacterial origin. Carbon isotopic compositions of Ct6:0 and Cls:0 exhibit similar trends with depth, but are significantly different in 613C values compared to other short-chain FAs (Fig. 7c), suggesting that C~6:0 and C~s:o are derived from sources other than bacteria, most likely from algae. These two FAs are generally the most abundant FAs in phytoplanktonic algae, and their 6~3C values are in a similar range as

planktonic sterols (-24 to -29%0) in the Santa Monica Basin surface waters (Hollander, unpublished data). Since bacteria can also synthesize C16:0 and Cls:O, the more enriched values of C16:0 and Cls:O may suggest dominantly algal source whereas the isotopically lighter Cl6:0 and Cis:o may be synthesized by bacteria in the sediments. As was pointed out before, the anoxic condition at this site may lead to better preservation of some of these algal FAs.

In the periphery sediments, all short-chain FAs exhibit smaller variations of 6~3C values with depth as a result of sediment mixing due to bioturbation (Fig. 7b,d). All the short-chain FAs have similar 613C values as bacterial Cis:0 and is'o-Cls:O (Fig. 7b). This may suggest that there has been a very strong recycling of organic matter by bacteria at this periphery site and that most short-chain FAs have been resynthesized by microbial processes in oxic sediments.

Significantly depleted values of short-chain bacterial FAs in the SMB sediments may be the result of being synthesized chemoautotrophically from very light carbon sources in the pore water or where the CO2(aq) concentration was high. Chemoautotrophic processes are occurring as evi- denced by the light isotopic composition of bishomohopanoic acids from both depocenter and periphery sediments ranging from -30 at depth to -45%o close to the surface (Fig. 7a,b) (Freeman et al., 1990; Prahl et al., 1992; Freeman et al., 1994). The slightly depleted values for most short- chain FAs could also be the product of anaerobic microorganisms exhibiting unique fractionation against the heavy isotope ¢3C). It has been noted by M. Teece (personal communication), however, that up to 10%o fractionation occurred between FAs (C16:~, CI6:0, Cls:~, and Ci8:o) synthesized by Shewanel la putre faciens and the culture substrate (lactate) when grown under anaerobic conditions, whereas essentially no fractionation was observed between these FAs of Shewanel la putre faciens and the substrate when grown aerobically.

Terrestrial organic carbon from river runoff at this region has 613C values ranging -23.7 to -26.4%o (Williams et aL, 1992). If lipids are 3-5%0 depleted than the whole cell or the bulk organic matter, FAs derived from these materials should have isotopic values of about -26 to 31%o. Most long-chain FAs from the sediment extracts have 613C values o f - 3 0 + 2%0 (Fig. 7e,f), indicating they could possibly be derived from terrestrial organic matter. However these values are also in the same range of bacterial FAs. As some bacteria have the ability to synthesize FAs with chain length of up to Cs0, bacterial contribution cannot be excluded. C26:0, C28:0, and C30:o have 613C values significantly more depleted than the possible range of terrestrial FAs, especially at shallow depth from both sites


(Fig. 7e,f), suggesting contributions from bacterial sources.

Based on two component mixing from terrestrial FAs (relatively heavier O|3C) and bacterial FAs (relatively lighter 313C), more depleted values for C26:o to C30:o could indicate that a higher proportion of these FAs are derived from bacteria than C24:o and C22:0. The alternative, more plausible, explanation is that a similar proportion of these long- chain FAs are derived from bacteria, but bacterial FAs have more depleted 613C compositions with increasing chain length from C22 to C30. This pattern of more depleted values with increasing chain length could be the result of enzymatic isotopic fractionation associated with desaturation and elongation along the pathway of long-chain FA biosynthesis from Cts:0 (Sedgwick, 1973; Nes and Nes, 1980). This fractionation pattern was observed by Fang et al. (1993) in the mytilids from Gulf of Mexico hydrocarbon seep communities. In this study, C20 FAs are 2-4%0 lighter than Cl6 acids, while C22 FAs are depleted by 2%0 compared to C20 FAs. Monounsaturated FAs are more depleted in ~3C than their corresponding saturated acids (i.e. 16:1 vs. 16:0), whereas the polyunsaturated FAs (i.e. 22:2) are depleted in 13C relative to mono- unsaturates.

In addition, the isotopic compositions of long- chain FAs vary from -30%0 at a depth of 165 mm to -44%o at the surface in the depocenter sediments (Fig. 6e). If these long-chain FAs were solely derived from terrestrial sources, this variation would imply either dramatic changes of drainage systems that had delivered these terrestrial materials or a recent increase in plant discrimination against heavy carbon. No major drainage system changes had occurred in the last two centuries along the southern California Coast. There is also no documented transition from C4 plants to C3 plants, a likely mechanism for vast changes of isotopic compositions of terrestrial organic matter. The input of light carbon into the atmosphere from fossil fuel burning only shifted the isotopic composition of atmospheric carbon dioxide by ~1%o (Mook et al., 1983; Keeling et al., 1984), thus this is unlikely to be the explanation of the variation of long-chain FA isotopic compositions. This further suggests that these long-chain FAs are a combination of terrestrial fatty acids and in situ biosynthetic products of microbial activities. Much more depleted values toward the surface for the depocenter sediments and at 15 mm depth for the periphery sediments may be the result of a much larger contribution from bacterial FAs at these intervals. The isotopic compositions of bishomohopanoic acids also decrease toward the surface in both settings, an indication of increasing contribution of chemoautotrophic bacterial biomass as the anoxic bottom

water expanded and increased in thickness in the depocenter site.

The above discussion points out that most of the short-chain FAs are sourced by bacteria, especially in the periphery site where aerobic bacterial decomposition and resynthesis have probably replaced most algal FAs. Long-chain FAs are sourced from a combination of terrestrial organic matter and bacteria, with the contribution from bacterial sources being higher in the depocenter site relative to the periphery site, and higher toward the sediment surface at both sites. Chemoautotrophic bacteria had an increasing contribution as the anoxic bottom water increased in its volume. Therefore, in contrast to the results derived from traditional source assignment, we propose that a significant portion of sedimentary FAs are sourced by bacteria, and that microbial processes may have played an important role in determining organic matter content and compositions in the SMB sediments.

Preservation o f algal and terrestrial FAs vs. contribution o f bacterial FAs

Due to the proximity of these two cores, both sites have experienced identical organic matter flux from the water column. The difference in organic matter quantity and quality and FA concentrations between these two sites could only be the result of the development of bottom water anoxia and associated chemical/biological processes in the depocenter site. Much higher concentrations for almost all FAs in the depocenter sediments, especially in the top several centimeters could be due to (1) higher degradation rates in oxic sediments and better preservation of FAs at the anoxic depocenter site, (2) higher contribution of FAs synthesized by in situ bacterial community at the anoxic depocenter site, or (3) a combination of the above two reasons.

It has been suggested by Claypool and Kaplan (1974) that anaerobic degradation is thermodynami- cally less efficient than aerobic decomposition, thus promoting higher preservation of organic matter under anaerobic conditions. From the source assignment (Fig. 8a,b), algal FAs have a higher contribution in the depocenter site than the periphery site, an indication of higher preservation in the anoxic bottom water. Carbon isotopic compositions of FAs also suggest that a stronger signature of algal FAs are preserved in the depocenter site (Fig. 7c). There is also a strong selective preservation of terrestrial long-chain FAs vs. short-chain FAs in the oxic sediments (Figs 5 and 8b). But the absence of characteristic polyunsaturated FAs from algal sources indicates very strong decomposition of algal materials at both sites.

Of the FAs contributed by algae, terrestrial organic matter, and dead bacteria, the unsaturated


FAs and the branched FAs would be degraded more rapidly than saturated FAs, resulting in decreasing ratios of unsaturated to saturated FAs with depth (Farrington and Quinn, 1973; Johnson and Calder, 1973; Parkes and Taylor, 1983; Haddad et al., 1992). However, the rather consistent ratios of the unsaturated to saturated FAs and the branched to straight-chain FAs for both depocenter and periphery sediments (Fig. 9a,b) indicate that preservation and different rates of decomposition cannot be the dominant cause of this pattern. Rather, the FA distribution is probably the result of contributions from an in situ bacterial community. The FA abundance vs. depth profile for the depocenter sediments may reflect a very high active bacterial biomass at the water/sediment interface and living bacterial communities at all depths. The diagenetic decomposit ion of these FAs with increasing depth may not be a major signal in this concen- t ra t ion-depth profile. The periphery sediment differs from the depocenter sediment by having a much smaller abundance of bacterial biomass at the water/sediment interface.

Higher abundance of bacteria in anoxic bot tom sediments at the SMB is also shown by the ATP concentration profile in the sediments (Fig. 10a,b) (Craven and Jahnke, 1992). The ATP concentration, indicative of active biological population in the environment, is almost two orders of magnitude higher at the sediment/water interface from the depocenter sediments than the basin slope sediment• Since the anoxic bot tom water prevents benthic macroorganisms from inhabiting the sediments, this

high ATP profile can only be the result of an active microbial population. Using the commonly inferred C:ATP ratio of 250:1 (Craven and Jahnke, 1992 and references therein), they estimated the living microbial biomass from the measured ATP concentration in the depocenter surface sediments, and this microbial biomass could account for up to 40% of the TOC. They then argued that this C:ATP ratio was too high, because this high microbial biomass contribution at the surface would require greater than a twofold depletion in the det- rital organic carbon content of the surface layer relative to the 10-20 mm depth horizon in order to explain the relatively uniform values of TOC throughout these depths. This concern seems to be unjustified, because active microbial biomass at the surface could well be preserved as possibly more recalcitrant bacterial necromass below the zone of intense microbial activity. In sediments from the highly productive Peru margin, Parkes et al. (1993) observed a decrease in the bacterial population and activity as the proport ion of uncharacterized, relatively recalcitrant organic matter increases. They hypothesized that if this material is being produced from bacterial biomass, then the rapid production of bacterial biomass/necromass would explain enhanced organic matter preservation in highly productive regions like Peru. Similarly Fossing (1990) noted that at high rates of anaerobic carbon utiliz- ation, there is enhanced organic matter preservation, which could be explained by production of a resistant bacterial necromass. Therefore, it cannot be ignored that there is a very strong contribution

5 0 -

1 0 0 -

E E 150- ¢.. E,

200-

250 -

300 -

350

D E P O C E N T E R SEDIMENTS r a t i o o f F A concentration

0 0.1 0.2 0.3 0.4 0.5

o

" 12.7:2:=:;.,

..!2:..~.:o • ::.~..o

ted/saturated

:~ ....... 0 ....... branched/straight a

50-

1 0 0 -

150 -

200 -

250 -

300 -

PERIPHERY SEDIMENTS ratio of FA concentration

0 0.1 0.2 0.3 0.4 0.5 1 I L i

Q ........... O

O:::::::2 ............ 1:7::=O

Fig. 9. Ratios of FA concentration are plotted against depth to illustrate the small variations of these ratios at different depths in both the depoeenter and periphery sediments. The ratios of unsaturated/ saturated are calcualted from FA Ci6:o, Ci6:lw7, C16:1w9 Ci8:0, Cl8:lw7, Ci8:1w9, C20:(}, C20:1, C22:1, and C22:0. The ratios of branched/straight are calculated from FA iso-Ci3:o, anteiso-Ct3:o, Ci3:0, iso-Cis:o,

anteiso-Cls:o, Cts:o, iso-CtT:O, anteiso-Ct7:o, CiT:O, iso-Cts:o, anteiso-C18:o, and Ci8:0.

Contribution of bacteria to sedimentary organic matter

DEPOCENTER SEDIMENTS

ATP ~tg/g

0 100 200 300 400 500 0

10-

~" 20

30

40

50

--O--- ATP

0 0

10

20

30

40

50

SLOPE SEDIMENTS ATP Ixg/g

2.5 5 7.5

Fig. 10. The concentration of adenosine tri-phosphate (ATP) extracted from the depocenter and the basin slope sediments (modified from Craven and Jahnke, 1992).

of bacterial biomass to the FA concentration profile in the depocenter site in addition to the enhanced preservation of algal and terrestrial FAs in the anoxic bottom water environment.

The importance o f chemoautotrophic bacteria

The isotopic composition of bishomohopanoic acids infers the presence of chemoautotrophic bacteria in the SMB sediments, and there is a higher contribution of these autotrophic bacteria in the depocenter site relative to the periphery site and toward the sediment surface. Triglycerides extracted from suspended particulate organic matter have very different isotopic compositions from different water depths: -28%o in the surface water (50 m water depth) and -46%o in bottom waters (859 m water depth) below the oxic/anoxic interface (Hollander, unpublished data). These triglycerides with very depleted 613C values could only be sup- plied by autotrophic microorganisms living at the oxic/anoxic interface using a very depleted carbon source or at a very high CO2(aq) concentration.

The significance of chemoautotrophic bacteria in this environment is that they can convert respired CO2 and dissolved organic matter into new biomass and increase the total organic carbon contents in the sediments. Beggiatoa, an autotrophic sulfur-oxi- dizing organism in marine and freshwater sediments (Henrichs and Farrington, 1984; Rheiheimer, 1985; Savrda and Bottjer, 1991; Sassen et al., 1993; Steenbergen et al., 1993) was observed to be widely spread as bacterial mat above the anoxic sediments in the nearby Santa Barbara Basin (Grant, 1991) and is responsible for increased sedimentary TOC contents. The fluctuation of Beggiatoa mat growth has also been suggested (Christensen et al., 1994; Reimers et al., 1990) to be the cause of sediment lamination in the central Santa Monica Basin. Combined with the possible chemoautotrophic bac-

559

teria growing at the oxic/anoxic interface in the water column, these autotrophs could supply additional organic matter and increase the organic matter contents in the underlying SMB sediments.

The influence o f bacterial processes and biomass on bulk organic matter characteristics

Isotopic compositions of bulk organic carbon exhibit a decreasing trend of up to 2%0 from 130 mm to the surface for the depocenter sediments (Fig. 7c), and parallel the decreasing ~13C trends in very long-chain FAs (C26:0 to C30:0) and bishomohopanoic acid (Fig. 7a,c). This correlation would have been better if the first two samples near the surface had not been analyzed for 6t3C on sediment residues from solvent extraction. This close correlation suggests that an increasing contribution of autotrophic bacterial biomass having very light isotopic compositions may also be reflected in the isotopic composition of bulk organic matter as the anoxic bottom water expands in its volume and thickness in the central basin. Even though such chemoautotrophic or even methylotrophic bacteria have been documented to contribute to the sedimentary organic matter based on isotopic values of biomarker compounds (Hayes, 1997 and reference therein), the isotopic compositions of those bulk organic matter do not have any significant reflection of this contribution, probably because the total autotrophic bacterial biomass contribution is very small in those cases.

Another characteristic of the organic matter in the depocenter sediments is that they have much higher H/C ratios than the periphery sediments and this ratio is increasing toward the sediment surface (Fig. 3b). This difference has been attributed to the development and expansion of anoxic bottom water in the depocenter site (Hollander et al., 1994). The above discussion has proposed that anoxic bottom


water in the depocenter site has better preserved algal- and terrestrial-derived organic matter and also promoted the growth of chemoautotrophic bacteria in the anoxic water column and anaerobic bacteria in the sediments. This autotrophic bacteria and anaerobic microbial biomass have significantly contributed to the sedimentary organic matter in the depocenter site. This increasing contribution of anaerobic and chemoautotrophic bacterial biomass with time could partly be the cause of the higher and increasing H/C ratios in the SMB depocenter sediments relative to the periphery sediments. Thus we suggest that the increased TOC accumulation rates and H/C values in the depocenter sediments is the result of a higher contribution of autotrophic and anaerobic bacterial biomass in addition to better preservation of organic matter enhanced by anaerobic bacterial transformation of these materials in the anoxic depocenter sediments than the periphery sediments at the Santa Monica Basin (Fig. 3a,b). Claypool and Kaplan (1974) have suggested that anaerobic degradation could result in more lipid- and hydrogen-rich organic matter than aerobic degradation. The study by Pratt (1984) also found a close association of high organic carbon content and hydrogen-rich organic matter with laminated sediments (no bottom water oxygen) and low organic content and a low oxygen index with macro- burrowed sediments in Cretaceous Greenhorn Formation. Other ancient petroleum source rocks, such as Lower Toarcian organic-rich sediments in the Paris Basin (Baudin et al., 1990) and the Kimmeridge Clay Formation (Miller, 1990) also have high TOC and hydrogen index, which are associated with an anoxic bottom water environment. Thus the role of anoxia to the organic matter accumulation in sediments is that it not only provides a condition for slower decomposition and higher preservation of organic matter, but it may also pro- mote the development of chemoautotrophic bacteria and the growth of anaerobic microbial biomass, which in turn considerably modify the chemical characteristics of organic matter and increase the total organic carbon accumulation. We suggest, therefore, that microbial processes can significantly change the quality and quantity of organic matter from anoxic settings both in recent and ancient sediments.

2.

3.

4.

5.

Basin sediments are sourced by bacteria as a result of active recycling of organic matter and resynthesis by the in situ bacterial community, especially in the aerobic decomposition condition at the periphery site. Long-chain FAs are also partially derived from bacteria. Much higher FA abundance in the depocenter sediments is the result of a higher bacterial biomass contribution and slower decomposition of algal and terrestrial FAs under anaerobic conditions. The presence of chemoautotrophic bacteria is indicated by the very depleted values of bishomohopanoic acids in the sediment extracts and triglycerides in particulate organic matter from the anoxic water column. We suggest that the combination of an increasing contribution of autotrophic and anaerobic bacterial biomass in the depocenter site, and the differential decomposition of sedimentary organic matter, causes the increasing differences in the organic carbon accumulation rates and H/C ratios between the basin depocenter and periphery and the decreasing ?JI3C of bulk organic matter in the depocenter sediments. Bottom water oxygenation exhibits a definite control on the isotopic and organic geochemical signature of organic matter preserved in sediments by regulating the ecology of microorganisms and the functioning of microbial processes in the Santa Monica Basin. Because of the ubi- quitous presence and the strong reworking and resynthesizing ability of bacteria at the sediment/ water interface and in the sediments, a significant contribution of bacterial biomass to sedimentary organic matter can be expected under anaerobic conditions. The implication of these results is that bacterial processes may play a significant role in determining the quality and quantity of ancient sedimentary organic matter regardless of whether water column and sediment anoxia resulted from higher surface water primary productivity or restricted circulation in basins.

CONCLUSIONS

This comparative study of sediments from locations with oxic and anoxic bottom waters in the Santa Monica Basin allowed us to assess quantitatively the role of bacteria and bottom water oxygenation in controlling the organic matter accumulation and composition in sediments.

1. Molecular and isotopic evidence indicates that most short-chain FAs from the Santa Monica

Acknowledgements--We would like to thank J. M. Hayes for the support of the water column and core collection portions of this study and for thoughtful discussions. In addition, we thank S. Howe for stable isotope analysis and analytical facilities management at NU, S. C. Brassell for the assistance with interpreting GC-MS data, and A. Schimmelmann for analytical assistance in the use of the GC-MS instruments at Indiana University. Many thanks also go to K. H. Freeman, R. Summons, and J. S. Sinninghe Damste for their critical review and valuable suggestions. This work was supported by a grant to D.J.H. from the Department of Energy's National Institute for Global Environmental Change (#21312-0051).


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