Distributions of uronic acids and O-methyl sugars in sinking and sedimentary particles in two coastal marine environments

Abstract

Although recent research has indicated that bacteria may contribute an important fraction of biochemical residues in terrestrial and marine environments, it is difficult for geochemists to identify contributions from these ubiquitous and biochemically diverse organisms. Previous studies have suggested uronic acids and O-methyl sugars may be useful indicators of microbial abundance and activity, but have been limited primarily to analyses of a small number of isolated samples. We report here comparative distributions of O-methyl sugars, uronic acids, and aldoses in sediment trap material and sediments from Dabob Bay, WA and nearby Saanich Inlet, BC, where temporal and spatial trends may be used together with well-established patterns in other biochemicals to identify bacterial contributions against the background of other carbohydrate sources.

O-methyl sugars and uronic acids were important contributors to the overall flux and burial of polysaccharide material in Dabob Bay and Saanich Inlet, composing ≤12 wt% of the total carbohydrate yields from sediment trap and sediment samples. O-methyl sugars accounted for an average of 5% of the carbohydrate yields from sediment trap materials and sediments, but were found rarely and only in low abundance in vascular plant tissues, phytoplankton, and kelp. In contrast, uronic acids were abundant products of sediment trap material and sediments, as well as vascular plant tissues, where in some cases they predominated among all carbohydrates. Uronic acid abundance in sediment trap material averaged 3% and ranged to >6% of total carbohydrate yields.

The persistence of total minor sugar yields in water column collections from Dabob Bay throughout the seasonal cycle indicated they had a primary source that was not directly related to plankton bloom cycles nor pulsed inputs of vascular plant remains. Subsurface maxima in total minor sugar yields (and several individual components) within sediment cores from both sites indicate in situ sedimentary sources. Taken together, the observed environmental distributions strongly suggest that the minor sugar abundances in Dabob Bay and Saanich Inlet were controlled by in situ microbial production.

Introduction

Carbohydrate polymers in their many diverse forms are the most abundant class of biopolymers on Earth, comprising over half of the organic material in the biosphere (Aspinall, 1983). Carbohydrates occur in high abundance in oceanic dissolved organic material Aluwihare et al 1997, McCarthy et al 1996, Benner et al 1992 and in the sea-surface microlayer Compiano et al 1993, Henrichs and Williams 1985. They are also central to many environmental processes such as the formation of humic substances (Yamaoka, 1983), removal of dissolved metals (Geesey et al., 1989), flocculation of dissolved organic material Eisma 1986, Mopper et al 1995, and adhesion of both soils (Cheshire, 1979) and marine sediments (Dade et al., 1990).

Most studies on the origins and fates of carbohydrates in the marine environment have been based on measurements of the relative abundances of “simple sugars,” usually defined as unsubstituted aldoses and ketoses Hamilton and Hedges 1988, Tanoue and Handa 1987, Cowie and Hedges 1984b, Ittekkot et al 1984, Ittekkot and Degens 1982, Mopper 1977. Identification of biologic and geographic sources of carbohydrate polymers from the relative abundances of these simple sugars, however, has been difficult due to their ubiquitous occurrence in living organisms and differential diagenetic reactivity Cowie and Hedges 1984b, Hedges et al 1988b, Macko et al 1989.

In addition to the simple sugars, however, there is great variety in the monomeric constituents of carbohydrate polymers. Many carbohydrate polymers—polysaccharides—are composed of mixtures of simple and minor sugars, of which, the latter are typically more source specific. These minor sugars, which occur in myriad forms, are distinguished from simple sugars in their substitution of one or more hydroxyl group with an alternate functional group (Aspinall, 1983). The types and proportions of minor sugars found in environmental samples may thus provide insight into the geochemistry of the total carbohydrate pool Moers 1993, Moers et al 1990a, Moers et al 1990b, Klok et al 1984a, Klok et al 1984b, Mopper and Larsson 1978.

This study examines two classes of minor sugars, uronic acids and O-methyl sugars. Uronic acids differ from aldoses in the replacement of the methanolic carbon opposite the carbonyl carbon with a carboxylic acid group. O-methyl sugars are aldoses or uronic acids with one or more hydroxyl groups replaced by an etherified methyl group. Klok et al. (1984a) identified >40 varieties of O-methyl sugars in Black Sea and Namibian shelf sediments. Moers et al. (1990a) found a similar complexity in a mangrove peat. An acidic polysaccharide, glucuronomannan, has been reported in deep-sea sediments (Handa et al., 1972). Mopper and Larsson (1978) found uronic acids, including 4-0 methyl glucuronic acid, in sediments from the Baltic and Black Seas. Uhlinger and White (1983) suggested that the uronic acid content of sediments is characteristic of their microbial biomass. Both compound types are particularly interesting as potential indicators of microbially derived polysaccharides in marine sediments Moers et al 1990a, Moers et al 1990b, Moers et al 1993, Klok et al 1984a, Uhlinger and White 1983, Fazio et al 1982.

Recent research in marine environments indicate that microorganisms and their remains contribute strongly to the organic material found in natural waters McCarthy et al 1998, McCarthy et al 1996 and sediments. The task of recognizing the microbial contribution is daunting, however, because microbial species are remarkably diverse, with only a small fraction that can be cultured for subsequent chemical analyses. Bacteria in particular are biochemically inventive and make a wide variety of biochemicals (intercellular and exuded) in changing patterns depending on immediate environmental conditions (e.g., Decho 1990, Wrangstadh et al 1986, Kenne and Lindberg 1983). Even if the full range of polysaccharides synthesized by all bacteria under different conditions were known, very little information exists on the relative sensitivities the component sugars to degradation. A major complication is that bacteria are the main agents of decomposition in marine settings and therefore can introduce new biochemicals in situ at almost any point during the diagenetic process. Thus, one practical approach at this early stage of study is to comprehensively survey minor sugars across diverse natural environments and processes to see if the observed distributions and abundances are consistent with microbial production.

Minor sugars are produced by nonmicrobial sources as well. Uronic acids are widely distributed in vascular plants and marine organisms (Whistler and Richards, 1970) and are the primary structural units in commercially important alginic and pectic acids (Painter, 1983). O-methyl sugars are common in soils (Ogner, 1980) and marine sediments (Klok et al., 1984a), are also components of algal (Painter, 1983) and bacterial polysaccharides (Kenne and Lindberg, 1980), and occur in low abundances in some vascular plant materials Stephen 1983, Bacon 1971.

Our study examines minor sugar distributions in a variety of potential sources, as well as in sediment trap and core materials from two coastal marine sites: Dabob Bay, Washington and Saanich Inlet, British Columbia. Both sites lack substantial direct river input and are similar in their surrounding terrestrial environments, vegetation, and rate and timing of plankton productivity. They differ principally in the depth of the sill that separates them from a tidally flushed channel, and consequently in water column oxygen levels. The Dabob Bay sediment trap samples were from a year-long series of monthly deployments that were examined previously for seasonal variability in the composition and fluxes of simple sugars (Cowie and Hedges, 1984b), lignin (Hedges et al., 1988a), and amino acids (Cowie and Hedges, 1992) and compared to the upper 50 cm of underlying sediment. Simple sugar, lignin phenol, and amino acid compositions of the sediment trap materials and varved sediments from Saanich Inlet analyzed in this study were also previously reported Hamilton and Hedges 1988, Cowie et al 1992.