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Carbohydrate dynamics and contributions to the carbon budget of an organic-rich coastal sediment

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Abstract

Potential hydrolysis rates of three different polysaccharides, pullulan, laminarin, and xylan, were measured in intact sediment cores from Cape Lookout Bight, North Carolina, in order to constrain the rates at which a fraction of the high-molecular-weight sedimentary carbon pool may be hydrolyzed to lower molecular weights. Potential hydrolysis rates of pullulan were somewhat higher than those of laminarin and xylan. Highest potential rates were measured in surface sediments; rates at depths of 5–7 and 14–16 cm differed relatively little from one another. Total dissolved carbohydrates, dissolved organic carbon (DOC), sulfate, and sulfate reduction rates were also measured and compared with data previously collected at Cape Lookout Bight in order to investigate carbohydrate dynamics and establish the relative contribution of carbohydrates to the sedimentary carbon budget. Total porewater carbohydrates constitute a disproportionate fraction of DOC, ranging from a maximum of 85% in near-surface intervals to 24% at depths of 14–16 cm. A comparison of potential hydrolysis rates, dissolved carbohydrate concentrations, DOC, and sulfate reduction rates, along with results from a wide range of studies previously conducted at this site suggests that hydrolysis of high-molecular-weight polysaccharides can potentially be very rapid relative to carbon remineralization rates. Dissolved porewater carbohydrates form a dynamic pool that is likely turned over on short timescales in Cape Lookout Bight sediments.

Introduction

In coastal sediments, where much organic matter remineralization is carried out under anoxic conditions Berner 1978, Jørgensen 1982, the concerted action of a diverse microbial community (a “microbial food chain”) is required to remineralize particulate organic carbon (POC) to CO2 and CH4. Large substrates must initially be hydrolyzed by microbial extracellular enzymes to smaller substrates that can be transported across bacterial membranes. Heterotrophic bacteria utilize the hydrolyzed substrates for cellular carbon and energy, and excrete organic transformation products. These products are then utilized by other members of the microbial food chain, which in turn further transform the organic carbon. The terminal members of the food chain, sulfate reducers and methanogens, generally utilize simple substrates such as short-chain fatty acids, oxidizing the carbon to CO2, with concurrent production of sulfide or methane (Gottschalk, 1986). The net activity of the microbial food chain is frequently quantified by measuring terminal processes such as sulfate reduction (e.g., Jørgensen 1982, Canfield et al 1993). More detailed characterizations of the organic carbon transformations carried out by members of the microbial food chain are hampered by significant analytical problems. Very little is known about the nature of the initial transformations of organic macromolecules or about the identities and activities of microbes that produce extracellular enzymes in sediments. Determining the rates and pathways by which organic macromolecules are transformed to the simple substrates ultimately utilized by sulfate reducers, and identifying key bottlenecks in the overall remineralization processes, remains a major challenge.

The purpose of this work is to apply a recently developed method Arnosti 1995, Arnosti 1996 to measure activities of specific extracellular enzymes in sediments of a well-characterized coastal ecosystem. These measurements can be used to constrain the rates at which a portion of the high-molecular-weight organic carbon pool is hydrolyzed to substrates sufficiently small to be utilized by successive members of the microbial food chain. By combining these data with measurements of sulfate reduction rates, this study helps illuminate the boundaries of carbon flow between the initial and terminal members of the sedimentary microbial food chain.

Cape Lookout Bight, North Carolina, where organic matter cycling has been intensively studied during the past 25 years, was selected as the study site. Rates of carbon oxidation, sediment accumulation, and POC and DOC turnover in sediments (e.g., Martens et al 1992, Alperin et al 1994) have all been determined, as have organic matter sources and organic carbon burial rates (Martens et al 1992, Canuel and Martens 1993 and references therein). Sedimentation in Cape Lookout Bight is rapid (10 cm yr−1), as are rates of carbon oxidation, which show reproducible seasonal changes linked to the annual temperature cycle Martens and Klump 1984, Crill and Martens 1987. In the summer, sulfate is usually depleted below 10 cm, and methanogenesis becomes an important terminal process in organic matter remineralization (Martens and Klump, 1984). DOC inventories also exhibit seasonal cycles linked to the transition between sulfate reduction and methanogenesis which occurs during summer months Burdige and Martens 1988, Alperin et al 1994.

A number of studies have focused on the dynamics of specific components of organic matter in Cape Lookout Bight sediments, particularly the amino acid pools Burdige and Martens 1988, Burdige and Martens 1990 and lipid pools Haddad et al 1992, Canuel and Martens 1993, Canuel and Martens 1996. For this study, carbohydrates were selected as the major focus, particularly because they comprise a significant fraction of Cape Lookout Bight sedimentary organic matter. Haddad (1989) determined that 23 ± 17% of sedimentary organic carbon in the Bight is derived from vascular plants; the remainder is algal/bacterial in origin. Carbohydrates are major constituents of all of these potential sources, as structural, storage, and/or membrane components Aspinall 1983, Cowie and Hedges 1984, Hamilton and Hedges 1988. In Cape Lookout Bight, total neutral carbohydrates comprise approximately 7–8% of total organic carbon (TOC) in the upper 10 cm of the sediments, with glucose as the major neutral hexose (∼27% of total neutral carbohydrates) and xylose as the most abundant pentose (∼9% of total neutral carbohydrates) (Haddad, 1989). Other than the work of Haddad (1989), however, little attention has been focused on carbohydrates in Cape Lookout Bight.

The aim of this study therefore is to fill this gap in the organic carbon budget of Cape Lookout Bight. Potential hydrolysis rates of three structurally different polysaccharides (pullulan, laminarin, and xylan) were measured at three depths (∼0–2 cm, ∼6–8 cm and ∼14–16 cm) in Cape Lookout Bight sediments. These polysaccharides were selected because they are components of marine algae and/or the activities of enzymes that hydrolyze these polysaccharides have been identified in marine bacteria Painter 1983, Antranikian 1992, Arnosti and Repeta 1994. The objectives were to determine whether the rates of hydrolysis were dependent on the structural composition of the polysaccharides, and whether there were detectable changes in rates of hydrolysis with depth. Both overall reactivity of organic matter and microbial activity have been shown to decrease with sediment depth in Cape Lookout Bight Crill and Martens 1987, Burdige and Martens 1988, Canuel and Martens 1996, factors that suggest that rates of extracellular enzymatic activity may also decrease with depth. Studies with the same polysaccharide substrates at other sites have found evidence of both depth- and structure-related differences in potential hydrolysis rates Arnosti 1995, Arnosti 1998. By coupling these measurements with measurement of total dissolved carbohydrates, DOC, POC, sulfate concentration, sulfate reduction rates, the solid-phase carbohydrate data of Haddad (1989), and a 25-year database of organic carbon dynamics at Cape Lookout Bight, we intended to determine the contribution of carbohydrates to the total organic carbon budget. A comparison of carbohydrate hydrolysis and terminal remineralization rates additionally helps to highlight several intriguing aspects of carbon cycling in the sediments of Cape Lookout Bight.

Section snippets

Study site and sampling procedures

Sediment cores were collected by scuba divers in March 1997 at station A-1 in Cape Lookout Bight, North Carolina (Martens and Klump, 1984) (water depth ∼ 7 m; water temperature 15°C.) The cores were held in a cooler and processed within 7 h of collection. The sediments were light colored in the surface layer (0–2.5 cm) and darker black below, with a strong smell of sulfides throughout cores. Similar profiles have been described by Chanton et al. (1987) at this site at the same time of year.

Hydrolysis measurements

Potential hydrolysis rates

All three FLA-polysaccharides were measurably hydrolyzed after 36 and 60 h of incubation (Fig. 1). Potential hydrolysis rates tended to be somewhat higher in surface sediments (0–2 cm) than in mid-depth (6–8 cm) or deep (14–16 cm) sections; differences in potential hydrolysis rates between mid-depth and deeper sections were smaller and more variable.

The highest potential hydrolysis rates were seen for pullulan surface sediments at 36 h; the lowest potential hydrolysis rates were seen in the

Rates and depth trends of polysaccharide hydrolysis in sediments of Cape Lookout Bight

Potential hydrolysis rates in surface intervals tended to be higher than rates measured in mid- and lower-depth intervals. Higher microbial activity levels in surface than in subsurface sediments is consistent with many previous observations of Cape Lookout Bight sediments (e.g., Sansone and Martens 1982, Crill and Martens 1987, Canuel and Martens 1996), as well as with the measurements of sulfate reduction rates made in this study. The potential hydrolysis rates of mid-depth and bottom samples

Acknowledgements

We thank Dan Albert for his helpful suggestions and assistance both in the field and in the laboratory, Steve Keith for aid with sample analyses, and Chris Martens for discussions. Marc Alperin and Dan Albert provided thoughtful reviews of a preliminary version of this manuscript. Funding for this project was provided by a UNC IBM Fund Award and an NSF grant (OCE-950-3487) to C. A., and a fellowship from the Danish Science Foundation (9600705 and 9601423) to M. H.

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