Seasonality in the fluxes of sugars, amino acids, and amino sugars to the deep ocean: Sargasso sea

Deep-Sea Research, VoL 3 I, No. 9, pp. 1057 to 1069, 1984. Printed in Great Britain.

0 1 9 8 ~ ) ! 49/84 $3.00 + 0.00

O 1984 Pergamon Press Ltd

S e a s o n a l i t y in the f l u x e s o f s u g a r s , a m i n o a c i d s , a n d a m i n o s u g a r s t o the deep ocean: Sargasso Sea VENUGOPALAN ITTEKKOT,* WERNER G . DEUSER~" and EGON T. DEGENS*

(Received 18 February 1983; in revisedform 4 January 1984; accepted I February 1984) Abztraet--The fluxes of sugars, amino acids, and amino sugars as released by acid hydrolysis were determined in the <37-pm fraction of samples collected during successive two-month sediment trap deployments in the deep Sargasso Sea (3200 + 100 m) from April 1978 to December 1981. All fluxes varied seasonally and in phase with the flux of the <37-gm fraction, which has been shown to vary in phase with primary productivity in the surface layers. During the investigation the fluxes were in the range of 0.03 to 1.7 mg m-Zd -t. They contributed 13 to 34% of the measured organic carbon, and 30 to 53% of the measured total nitrogen could be accounted for by amino acids and amino sugars. The relative abundances of sugars and amino acids were, in general, similar to those reported for mineralized tissues of carbonate and silica producers and the cell walls of nonbiomineralizing organisms. However, the amounts of non-protein amino acids, i.e., [3-alanine and y-aminobutyric acid, of aspartic and glutamic acids, and of amino sugars relative to total amino acids varied seasonally. Relative abundances of these compounds appear to indicate the nature and source of organic matter arriving at the sediment trap.

INTRODUCTION

PARTICLEinterceptor traps in mid-water (sediment traps) provide a unique means for observing sedimentation processes and for directly measuring the fluxes of materials to the sea floor (SoUTAR el al., 1977). Recent studies on particle fluxes with the help of sediment traps have provided significant information on the nature and quantity of the fluxes (HONJO, 1978; U RREREand K NAUER, 1981 ; D EUSERel aL, 1981). It appears that significant information concerning the transport and transformation processes involving the material flux to the deepocean environment can be obtained by examining in detail the organic constituents associated with them (WAKEHAMet al., 1980; GAGOSlANel aL, 1982; LEE and CRONIN, 1982). We have examined the sugars amino acid, and amino sugar composition of materials collected during sediment trap deployments in the deep Sargasso Sea. METHODS

The samples were collected during successive sediment trap deployments in the Sargasso Sea over a period of more than 3~ years (April 1978 to December 1981; Table 1). The trap was moored 45 km southeast of Bermuda 3200 + 100 m below the sea surface and 1000 rn

* Geologisch-Paliontologisches Institutund M u ~ u m , Universitit Hamburg, Bundesstrasse 55, 2000 Hamburg 13, Federal Republic of Germany. ~"Woods Hole Oceanographic Institution,Woods Hole, M A 02543, U.S.A.

1057

V. l'r'rEKKOTetaL

1058

Table I. Sample numbers, collectionperiod,and duration of sediment trap deploymeats at 3200 + 100 m in the Sargasso Sea

Sample no.

Collectionperiod

Duration (days)

1 2

04/06/78-06/07/78 O6/O7178--O8108178

3 4 5 6 7 8

08109/78-10/10/78 12/12/78-02/14/79 03/24/79-05/31/79 05/31/79--07/30/79

62 62 62

02/06/80-04/07/80

64 68 60 61 61

63

12/05/79--02/04/80

9

04/15/80.-06/17/80

I0

06/20/80-08/I 1/80

52

11

08/11/80-10/14/80

64

12 13

10117/80-I 2/09180 12/I0/80-02/03/81 02/05/81-04/07/81

53 55 61

16 17

04/08/81--.05/26/81 05/27/81-07/21/81 07/21/81-09/15/81

18

09/I 7/81-12/02/81

48 55 56 76

14 15

above the sea floor to keep well above sediment resuspension. The trap is similar to the one described by H o m o (1978) and has a collection cross section of 1.54 m 2. The collection cup is closed during ascent and descent. Details of the deployment are described by DEUSER et al. (1981). No preservative or poison was contained in the collection cup. However, the results indicate that loss or degradation of the trapped materials did not significantly distort seasonal signals of source materials arriving in the deep ocean. Upon recovery and transfer into a bottle, the samples were stored in seawater and kept under refrigeration until laboratory processing began, usually within 2 to 4 days. The samples were then separated into various size fractions by washing them through a set of stainless steel sieves. Organic carbon, nitrogen, sugars, amino acids, and amino sugars were determined on dried, homogenized aliquots of the <37-ttm fraction. To check for the loss of organic matter during processing, a sample of water used for sieving and subsequently centrifuged off the <37-~tm fraction was analyzed. Routine analytical techniques for sediments and particulate matter were used. For a detailed account see MICH^EUS and IYrEKKOT(1982). Carbon and nitrogen were determined using a Carlo Erba Elemental Analyzer after treatment of the sample with dilute hydrochloric acid to remove carbonates. For the determinations of amino acids a few milligrams of each sample were hydrolyzed with 6 N HC! under nitrogen at 110°C for 22 h. One ml of the hydrolysate was evaporated to dryness and the residue taken up in a sodium citrate buffer of pH 1.8. A subsample was analyzed on a Biotronik Amino Acid Analyzer (GARR^Sl et aL, 1979). Analytical errors calculated from repeated analyses of known amounts of a standard amino acid mixture are given in Table 2. We also checked for the contribution of bacterial cell walls by analyzing muramic acid concentrations in some of the samples. This was done by hydrolyzing the sample with 4 N HCI at 100°C for 30 rain and processing the sample on a conventional amino acid analyzer. Muramic acid eluted between serine and gulamic acid. To determine sugars the samples were hydrolyzed with 2 N HCi at 100°C for 3.5 h under

1059

Fluxes of sugars, amino acids, and amino sugars in the Sargasso Sea Table 2.

Analytical precision of individual amino acids based on analyses using a standard amino acid mixture

Amino acids Cyst Asp Thr Ser Glu Gly Aia Val lie

s.d. (%)

Amino acids

s.d. (%)

2.8 4.6 6.3 10.4 4.1 6.7 7.0 5,6 2.7

Leu Tyr Phe I~-Ala y-Aba Orn Lys His Arg

6.9 7.8 5.9 6.7 7.3 16.4 5. I 5.9 2.6

50

40

g

0.2~

co,b~

]~ rl

Fig. I. Seasonal changes in total flux and the fluxes of organic carbon, nitrogen,carbohydrates, and amino acids (includingamino sugars) in the <37-gin fractionof materialscollectedduring sediment trap deployments at a depth of 3200 _ 100 m in the Sargasso Sea. Data point for sample 13 is not included for lack of flux data.

1060

V. ITTEKKOTet al.

nitrogen. The h y d r o l y s a t e was then desaited by electrodialysis using ion exchange m e m b r a n e s (JOSEFFSO~, 1970). The desalted samples were e v a p o r a t e d to dryness and the residues taken up in a small volume o f double-distilled water. A subsample was analyzed for sugars on a Biotronik S u g a r A n a l y z e r (MOPPER, 1977, 1978). Total sugars, a m i n o acids, and amino sugars were calculated as the sum o f individual sugars, a m i n o acids, and a m i n o sugars, which were identified and quantified. RESULTS T h e results are given in Fig. 1 and Tables 3 and 4. All fluxes show distinct m a x i m a between J a n u a r y and June o f each year. Organic constituent fluxes closely follow the total flux o f material in the < 3 7 - p r o fraction. Although the m a x i m u m sediment flux for the year 1981 was during the s a m e period as in 1979 a n d 1980, it was significantly larger. During the investigation the fluxes o f organic c a r b o n and nitrogen in the <37-1~m fraction varied between 0.3 and 4 m g m -2 d -! a n d 0.1 and 0.46 mg m -2 d -~, respectively. The sugars and amino acids a n d a m i n o sugars were in the range o f 0.03 to 0.64 m g m -2 d - ' and 0.12 to 1 . 7 m g m -~ d - I , respectively. The c a r b o n :nitrogen ratios ranged between 8.3 and 12.9 with an average o f 10. In the s u g a r spectra, individual monomers, i.e., glucose, galactose, and m a n n o s e d o m i n a t e d . H o w e v e r , rhamnose, fucose, arabinose, and xylose contributed significantly to the identified s u g a r fraction. The spectra o f amino acids were d o m i n a t e d by glycine, aspartic acid, glutamic acid, a n d lysine, generally in that order. Arginine was present in a m o u n t s a r o u n d 5%. G l u c o s a m i n e and galactosamine were identified and quantified in the samples and the a m i n o acid : a m i n o sugar ratios varied seasonally (Fig. 2). The non-protein amino acids

Table 3.

Distribution o f sugars in mole % in samples collected during sediment trap deployments at 3200 + 100 m in the Sargasso Sea

Sample no.

Rha

Rib

Man

Ara

Fuc

Gal

Xyl

GIc

Total (rag g-i)

I 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

9.4 9.3 8.1 8.1 9.3 8.2 8.5 8.0 9.3 11.7 8.4 8.6 10.0 9.6 11.6 9.3 10.9 9.1 10.2

0.5 0.3 2.6 3.5 2.3 2.0 4.4 4.6 4.5 3.5 4.4 3.8 1.9 1.4 2.1 4.5 0.3 4.2

17.6 22.4 13.4 16.1 17.0 12.3 18.2 19.1 20.1 19.8 19.2 19.3 21.5 18.5 18.2 17.3 13.7 13.7 18.3

7.7 4.1 7.9 8.0 7.8 9.0 7.7 7.9 8.1 6.5 8.6 8.3 7.0 5.6 7.0 7.7 7.0 8.3 10.5

9.9 4.7 20.1 11.6 10.2 10.2 11.7 11.0 10.6 8.3 10.7 10.9 11.4 8.6 10.6 10.7 10.7 10.1 11.4

20.9 17.4 22.2 21.0 20.3 21.0 20.7 20.8 18.5 17.7 18.6 18.9 20.6 20.4 22.4 20.5 22.3 21.5 15.0

8.9 7.8 9.9 12.0 1i.7 10.5 12.2 12.4 12.3 10.3 10.7 12.4 9.0 7.9 9.3 12.5 10.8 10.3 5.3

24.8 33.6 26.1 19.5 21.3 26.7 16.6 15.9 16.5 21.1 19.0 18.1 19.9 25.0 18.4 16.6 20.4 22.9 29.3

5.0 4.27 5.15 6.92 5.86 3.49 6.39 7.31 6.16 5.24 5.36 4.98 6.82 4.99 7.5 7.1 6.02 5.02 0.60*

Rha, rhamnose; Rib, ribose; Man, mannose; Ara, arabinose; Fuc, fucose; Gak galactose; Xyl, xylose; GIc, glucose. The data do not include fructose, which was also identified in the samples. Part of the fruotose is destroyed during the hydrolytic treatment. Sample numbers as in Table 1. The centrifugate is assigned No. 19. * -- gg I-I.

24 24 30 29 23 29 19 25 15 16 23 36 27 26 28 28 29 23 24

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

123 121 123 120 122 124 124 122 118 117 113 127 120 123 123 125 122 116 101

Asp

80 79 77 80 75 80 55 80 73 49 46 48 80 52 50 49 49 48 76

Thr

80 75 71 72 71 80 63 70 69 71 62 69 76 73 78 70 78 73 69

Ser 107 108 108 110 114 II0 114 111 113 105 106, 100 110 103 102 102 103 102 137

Glu 160 163 174 157 155 166 138 154 163 156 159 160 157 151 143 158 156 163 115

Gly 79 83 82 83 85 83 86 83 86 79 84 73 78 81 80 77 79 83 99

Ala 35 36 33 36 40 34 34 33 36 34 33 31 32 30 31 29

30 29 49

-

-

-

42

68

lie

6 -

Met

66 48 46 47 69 48 58 49 55 56 42 37 45 38 59 37 41

Val

47 46 81

46

50 52 46 50 58 48 52 49 54 54 47 44 49 47 52

Lcu 16 13 9 12 18 8 21 18 24 23 17 13 19 20 22 19 17 18 23

Tyr 29 29 29 30 32 28 31 31 32 31 29 30 30 30 33 30 30 30 35

Phe 15 16 17 16 I0 16 12 13 13 13 17 21 12 14 13 18 17 18 2 10 lO -

7 8

7 7 9 7 5 7 7 7 6 7 8 10 7 9 57 76 74 78 62 70 128

89 72 109 154 130 85 130 109 130 122 125 47

1

1 2 2 2 1 1 6 6 II II 2 6

Lys

2 5 2 4 2 4

[3-Ala y-Aba Om

9 12 16 9 11 7 II 10 12 13 13 14

9

8 10 9 9 II 9

His

54 55 57 56 48 55 47 55 54 50 49 55 52 52 51 52 52 50 52

Arg

11.80 13.43 10.83 12.63 14.97 11.26 15.70 11.75 12.96 21.77 10.77 12.14 13.02 18.81 17.12 27.38 15.41 14.99 0.75*

Total (rag g-l)

0.87 0.89 0.78 0.83 0.74 0.81 1.59 0.78 0.73 1.93 0.78 0.99 1.25 1.87 1.68 2.61 !.55 1.47

AS (rag g~-1)

Cys, cysteic acid; Asp, aspartic acid; Thr, ~'~eonine; Set, ~ ' i n e ; Glu, glutamlc acid; Gly, glyclne; Ala, alanine; Val, valine; Ile, isoleucine; Leu, leucine; Tyr, tyrosine; Phe, phenyl ahm/ne; ~ala, #-alanine; 7-Aba, 7-aminobuWric acid; Orn, ornlthine; Lys, lysine, His, histidine; Arg, arginine; AS, amino sugars. Sample numbers as in Table I. The ce~tr/flq~te is assigned No. 19. * = ~gl -I .

Cys

D~trlbutionofamlno acldsandamino sugars inre~duesper lO001nsamplescollectedduring sediment trap depioymen~at 3200 + lOOmtnthe SargassoSea

Sample no.

Tab~4.

1062

v. ITTEKgOT et al.

30

25

15

I,°1 15' < 10. Illllllllllllllllllltlliltllllllilllllllltllllil JFMAMJJASON JFMAMJJISONOJIMANJ,JASON JFNAHJJASON 1978 9 1979 [ 1980 C~ 1981 Cl

Fig. 2. Seasonal variations in the ratios of glutamic acid :~-aminobutyric acid (GLU :y-ABA), aspartic acid :l~-alanine (ASP:~ALA) and amino acids:hexosamines (AA:HA) of the organic matter contained in the <37-gm fraction.

Table 5.

Amino acids (AA) and amino sugars (AS) as percentage o f organic carbon and nitrogen. Amino sugars as percentages o f carbon. The ratios of amino acids :sugars are also given

Sample no.

AA-C

AS-C

S--C

AA-N

AS-N

AA : S*

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

8.80 10.50 8.68 10.12 11.12 9.91 12.39 8.96 10.68 17.40 8.50 11.49 10.25 13.72 15.52 26.17 14.52 12.19

0.52 0.55 0.49 0.52 0.42 0.56 0.96 0.46 0.46 1.18 0.47 0.74 0.77 1.05 1.17 1.94 1.16 0.93

3.60 3.16 3.98 5.30 4.10 2.95 4.68 5.29 4.76 3.89 3.95 4.49 5.15 3.42 6.35 6.48 5.51 3.84

39.27 35.96 37.28 37.47 35.53 32.45 39.27 30.43 29.95 52.80 29.79 40.26 34.36 44.99 50.73 86.25 46.24 48.43

1.56 1.27 1.37 1.91 0.96 1.25 2.15 1.07 0.'91 2.48 1.11 1.73 1.71 2.34 2.66 4.30 2.48 2.47

2.36 3.14 2.10 1.82 2.55 3.22 2.45 1.60 2.10 4.15 2.00 2.43 1.90 3.76 2.28 3.85 2.55 2.98

* Calculated from concentrations given in Tables 2 and 3.

Fluxes of sugars, amino acids, and amino sugars in the Sargasso Sea

1063

13-alanine and y-aminobutyric acid were also present; their amounts relative to aspartic and glutamic acids also varied seasonally, Thirteen to 34% of the organic carbon measured was accounted for by sugars, amino acids, and amino sugars, and 30 to 53% of the organic nitrogen was accounted for by amino acids and amino sugars (Table 5). However 86% of the nitrogen in one sample was contributed by these compounds. The total nitrogen contributed by amino acids, amino sugars, and ammonia added up to 107%, a value that may be due to contamination during processing. The ratios of amino acids : sugars also fluctuated between 1.6 and 3.85 (Table 5), roughly in phase with the flux of materials in the <37-pm fraction. The determinations of amino acid and sugar in the water sample used for sieving and subsequently centrifuged off the <37-gm fraction (Tables 3 and 4) indicated that <7% of the nitrogen and 18% of the amino acids and carbohydrates are lost to the dissolved pool. DISCUSSION

Studies of samples collected during the same experiment (DEuSER and Ross, 1980; DEUSER et al., 1981) showed that the fluxes of materials to the deep Sargasso Sea vary in phase with

primary productivity in the surface layers. The studies concentrated on the variations in the fluxes of organic carbon and iithogenic materials. It was also shown that the flux of materials in the <37-~tm fraction varied in phase with primary productivity. Seasonality in sediment fluxes appear to be characteristic of other deep-sea environments, as was shown during sediment trap experiments in the Panama Basin (HoNJo, 1982). The studies indicated that the transport of materials into the deep water takes place on rapidly sinking macroaggregates (McCAvE, 1975) like fecal pellets (HoNJo and ROMAN, 1978). In the following discussion we concentrate on the variations in the distribution patterns of sugars, amino acids, amino sugars, and their fluxes. Sugar and amino acid fluxes into a deep-water trap were measured directly by WEFEa et al. (1982) for circumpolar waters of the Drake Passage. In their deepest trap (2450 m) sugars, amino acids, and amino sugars totaled 36% of the organic carbon; 55% of the nitrogen could be accounted for by ammonia, amino acids, and amino sugars. In yet another study LEE et al. (1983) reported that amino acids made up to 15 to 35% of the total organic carbon flux and 35 to 75% of the total nitrogen flux. In the trap moored at 3200 m in the Sargasso Sea 13 to 34% of the organic carbon could be accounted for by sugars, amino acids, and amino sugars, and 30 to 53% of the nitrogen could be accounted for by amino acids and amino sugars during the deployment period (Table 5). The nature of the uncharacterized organic carbon and nitrogen is unknown. Some of the organic carbon could be in the form of wax esters, iipids, and phospholipids (WAKEHAM et al., 1980). Amines such as urea involved in the formation of marine 'humus' (DEeENS, 1970) or fixed to clay particles may also contribute to the measured nitrogen flux. Furthermore, as land-derived materials represent a part of the abiogenic particle flux (DEUSER et al., 1981 ; DEusEg el aL, 1983) it is conceivable that soil-derived organic matter attached to clay also contributes. Incomplete extraction may account for some of the missing organic carbon and nitrogen. Other classes of organic compounds associated with eolian dust (SIMoNEIT, 1977) may also reach the sea surface by dry or wet fallout. Their subsequent removal via biological agents to the deep water is conceivable. Future studies on stable isotopes and specific organic compounds with distinct terrestrial signatures should elucidate the question of a major terrestrial component.

1064

V. ITTEKKOTetal.

Sugars and amino acids as source indicators

Generally sugars and amino acids comprise 40 to 80% of most organisms and, as a consequence, represent a large part of the organic input to aquatic environments (DF.~3ENSand MoPPEg, 1976). They are primarily associated with structural components---biominerals--of the organisms. Biominerals are composed of inorganic (mineral) and organic phases. The organic phase acts as a template on which epitaxial growth of the mineral phase proceeds. Sugars and amino acids act as templates in the biominvralization of silicate, phosphate, and carbonate minerals [sec DFo~.Ns (1976) for a review]. The 'utility" of sugars and amino acids as biochemical markers stems from the fact that species-specific patterns exist. The major input of organic matter in the marine environment is in the form of shells, tests, and frustules of calcareous and siliceous organisms. Relative inputs from the various sources can be ascertained from the distribution pattern of specific sugars and amino acids. For example, ratios of sugars: arabinose to fueose and of the amino acids: aspartic acid to glycine can be used to distinguish between inputs from silica and carbonate producers. Although they are constituents of both silica and carbonate producers, the ratios of arabinose to fucose, aspartic acid, and glycine in the mineralized tissues are reversed with arabinose and aspartic acid dominating the organic matter associated with carbonate producers. The amino acid:hexosamine (AA:HA) ratios indicate the relative inputs from phytoplankton and zooplankton, especially crustaceans. Although the peritrophic membranes of fecal pellets of crustaceans contain minor quantities of hexosamine (FoRgrER, 1953), it is probably insignificant in comparison with the amount of chitin present in the whole crustacean (RAvMOter et al., 1969). A dominant input from crustacean remains will shift the ratio in favour of hexosamines. A second group of indicators concerns the microbially and abiotically mediated transformation of the organic matter within the water column and in sediments. The non-protein amino acids ~-alanine, y-aminobutyric acid, and ornithine are products of decomposition of aspartic acid, glutamic acid, and arginine, respectively. Variations in the amounts of these amino acids in deep-sea tripton may reflect the degree of microbial reworking of organic matter in the biologically active surface layers. Spectra o f sugars and amino acids

The sugar spectra are similar to those reported in cell walls of marine phytoplankton (HEcKV et aL, 1973) and in particulate matter collected from the deep-sea environment (H^~D^ and TOMINAGA, 1969). They are poorer in glucose than marine particulate matter collected near the surface during plankton blooms (ITTEKKOT et al., 1982). It has been suggested that polymers of glucose are lost to the dissolved pool from living cells during grazing by zooplankton or by lysis of cells suspended close to the boundary layers in midwater. Enrichment of structural polysaccharides in dissolved organic fractions at pycnocline boundaries has been reported by LmnEZErr et al. (1980). Prolonged suspension in the microbially active surface layers can lead to decomposition of even structural polysaccharides (H-rEKKOT, 1982). Rapid removal of such particles to deeper layers will protect them from further decomposition. Removal of intact phytoplankton consolidated in fecal pellets occurs (SCHg^DEg, 1971). Electron microscopic investigations of the materials collected in our traps have shown phytoplankton detritus, indicating arrival at the trap in larger, rapidly sinking aggregates (M¢C^vE, 1975) such as fecal pellets (HONDOand ROMAN, 1978). The observed depletion of glucose in the collected materials relative to that of living phytoplankton

Fluxes of sugars, aminoacids, and aminosugars in the Sargasso Sea

1065

may also have resulted from the loss of cell contents rich in glucose polymers due to cell lysis within the trap or during sample processing (GARDNERet al., 1983). Carbohydrate monomers such as mannose, rhamnose, and xylose are important building blocks of polysaccharides associated with biomineralizing organisms (KRAMPlTZand WlTT, 1979). In addition, fucose is an important constituent of silica cell walls (diatoms) (HECKYet al., 1973). Although its role in the biomineralization of carbonate producers is unknown, arabinose appears to be ubiquitous in the remains of such organisms (1TrEKKOT,198 I). In general, the observed distribution pattern of sugars suggests that the sugar monomers are derived from biomineralized tissues of carbonate and silica producers and the cell walls of non-biomineralizing organisms. The amino acid spectra are dominated by glycine, aspartic acid, and glutamic acids, which constitute 30% of the total amino acid and amino sugars. A distn'bution pattern similar to that found in our trap materials is also observed in particulate matter collected from the deep sea (DEGENS, 1970; SirEN and MACUE, 1978). The acidic amino acids, aspartic and glutamic acids, are instrumental in carbonate tissue formation (DEGENS, 1976). In addition, these amino acids are also easily adsorbed onto carbonate particles from the dissolved organic carbon pool in seawater (CASTERand MITrEREg, 1978). Amino acid distribution patterns in Recent foraminifera and radiolarians show the dominance of glycine and aspartic acid (KING, 1974). However, the relative abundances of the amino acids are reversed in these organisms, with aspartic acid dominant in foraminifera and glycine in radioladans. Similar enrichment of glycine relative to aspartic acid was also found in diatom cell walls by HECKYet al. (1973). In all our analyzed samples glycine was in higher amounts than aspartic acid. This, in conjunction with the distribution of fucose and arabinose, suggests dominance in the input of silica mineralizing tissues to the <37-1tin fraction of the sediment trap material. Bacteria colonize sediment trap materials (LEE et al., 1983). Judging from the analyses of muramic acid in some of our samples the contribution of bacterial cell walls seems to be < 1%. Muramic acid forms part of the murein present in bacterial cell walls in amounts of 950%. (LEHNXNGEg, 1975). The low values observed by us may be caused by the removal of unattached bacteria colonizing the sediment trap particles during sample processing (G^RDNEa at al., 1983). The loss of 7% of organic nitrogen and 18% of the sugars and amino acids to the dissolved pool during sample processing may be a further indication of this. Comparison of the amino acid composition of the sediment trap materials with those of marine particulate matter collected from the Pacific by conventional techniques (RITTENBERG et al., 1963; DEOENS, 1970) shows our samples to be depleted in ornithine. Ornithine is a decomposition product of arginine, and its absence from our samples indicates the relative freshness of the material collected. Furthermore it would not have been derived from the macroaggregation of dissolved organic matter, in which ornithine is one of the major amino acids (DEGENS, 1970). Conventional sampling techniques are liable to collect only smaller particles with low settling velocities and longer residence times in the water column. This in turn will increase the degree of decomposition of the particles, which is reflected in the relative enrichment of ornithine. However, in a recent study SIEZENand M^~3UE(1978) failed to detect ornithine in particulate matter from oceanic and coastal waters of the Pacific. Thus the possibility that the indication of ornithine in earlier analyses was an artifact of the analytical techniques cannot be ruled out. Nature o f organic matter

Further information on the nature of organic matter arriving in the trap can be obtained from the distribution of minor constituents in the amino acid fraction. Especially significant in

1066

v. i'ITEKKOTet al.

this regard is the presence of non-protein amino acids, 13-alanine and ~,-aminobutyric acid; these are absent from uitracleaned foraminerai tests collected from deep-sea sediments, which made SCrmOEDER(1975) term them "external amino acids". They are generally thought to be decomposition products of aspartic and glutamic acids, respectively. However, SCHROEDER (1975) found no evidence for their production during studies on either Recent foraminifera or various proteins in buffered solution. Thus it appears that their presence in sediments from the natural environment is related to enzymatic decomposition of aspartic and glutamic acids. Such decomposition can take place either on particles (LEE and CRONIN, 1982) or in the guts of organisms. I~-Alanine and "y-aminobutydc acid have been found in materials collected during sediment trap deployments in the surface layers of productive areas (LEE and CRONIN, 1982). It has been suggested that microbial degradation is slow in the deep-sea environment (J ANNASCHet aL, 1971); their presence in our samples is probably a reflection of the degree of microbial reworking of organic matter in the near-surface waters or in the digestive tracts of organisms (see below). In addition, WEFERet al. (1982) have shown that most of the degradation of polypeptides takes place at depths above 1000 m and that flux changes below this depth are much slower. A major problem with the above approach is the uncertainty concerning the nature and extent of degradation of organic matter within the traps. GARDNERet al. (1983) showed that loss of organic matter from the trapped materials can take place by decomposition, cell lysis, or leaching. Although their results are significant, we feel that they cannot directly be compared with those presented here. LEE et aL (1983) suggested that the organic substrates used by GARDNERet al. (1983)----lobster shell, squid pens, and zooplankton--may not be wholly representative of the natural particles settling to the deep sea. Our data on sugars and amino acids show that the organic matter associated with settling particles is mainly structural components. Furthermore, our results indicate that the loss of organic matter by the processes described by GARDNERet aL (1983) are not large enough to mask seasonal signals of the surface processes being recorded at a depth of 3200 m. In Fig. 2 are plotted the ratios of aspartic acid:~-alanine and glutamic acid:y-aminobutyric acid as possible indicators of microbial reworking of organic matter in the surface layers. The ratios fluctuate roughly in phase with the variations depicted in Fig. 1. During high flux periods the amount of non-protein amino acids is low relative to aspartic and glutamic acids. Expressed differently, organic matter arriving at the trap during high flux periods--related to surface productivity peaksNis less microbiaily degraded than that at other times. The seasonal fluctuations apparent in the amino acid and sugar ratios (Table 5) also suggest the 'freshness' of the settling materials. The fluctuations, together with the nature of sugars and amino acids, suggest that material collected in the sediment traps during these periods has been transferred rapidly from the surface layers. The observed amino acid distributaon pattern in our samples differs from that reported by WHELAr~(1977) for surface sediment samples from the Atlantic abyssal plain. The nonprotein amino acids I~-alanine and y-aminobutyrie acid contributed significantly to the amino acid spectra of those sediments. This probably indicates the intensity of microbial and benthic reworking of the incoming materials at the sediment-water interface and not in the deep water column. Amino acid:amino sugar (hexosamine) (AA :HA) ratios

The variations in the AA : HA ratios are plotted in Fig. 2. Whereas A A : HA ratios varied in phase with the flux of materials from the surface layers from 1978 to 1980, they remained

Fluxes of sugars, amino acids, and amino sugars in the Sargasso Sea

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nearly constant throughout 1981. Hexosamines were present in higher amounts relative to amino acids than in previous years. This may have been caused by a greater contribution of crustacean remains. The high percentage of hydrolyzable amino acids in the total organic fraction also favours such an explanation. RAYMONTetal. (1969) reported the protein content of zooplankton to be higher; this is especially significant because we observed an anomalously large flux in 1981. The C :N ratios and the distribution of the major sugars and amino acids during the period did not differ significantly from those from previous years. The flux peak of 1981 occurred during the same months as in previous years, i.e., between January and June, the period of peak surface productivity (MENz~ and RrrnER, 1961). We cannot explain what caused the increased input of crustacean remains in 1981. From data presented here and the observations of lithogenic flux (DEusEg et al., 1983) it appears that the peak flux originated in the surface layers and that organic geochemical indicators may be used to trace the origin of the flux. One might expect such fluctuations to be smoothed out by burrowing organisms in fully oxygenated waters, yet in areas of restricted circulation, such fluctuations would be preserved in the sediment record, as was shown for Black Sea sediments (DEOENSand MOPPER, 1976). General conclusions

The results show that the seasonality previously observed in the fluxes of materials into the deep sediment trap (DEUSERand Ross, 1980; DEUSERet al., 1981) can also be discerned for classes of compounds such as sugars, amino acids, and amino sugars. Significance of the influx of organic matter in fulfilling the energy requirements of benthic organisms has been shown by HIN¢;^ et al. (1979). We show that there is a seasonality in the influx of fresh, and hence 'edible', organic matter associated with primary productivity in the surface layers. Seasonal growth and reproduction patterns observed in benthic organisms (LIC~TFOOTet al., 1979) may therefore be triggered by seasonal flux of food from the productive surface layers. The biochemical interpretations offered here suggest the role of Zooplankton in the transport of materials to the deep sea as exemplified by the Sargasso Sea.:These and earlier studies on samples from the same sediment trap experiment (DEUSEg and Ross, 1980; DEUSEget al., 1981) indicate that zooplankton populations, through their active (fecal pellets) and passive (skeletal and tissue remains) products, are instrumental in the transfer of materials into the deep ocean and play a significant role in modern deep-sea sedimentation. Absence of this major biological agent in ancient sedimentary environments before the advent of zooplankton appears to constitute an essential difference between sedimentation processes of the prezooplankton and zooplankton eras.

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