Interaction of photochemical and microbial processes in the degradation of refractory dissolved organic matter from a coastal marine environment

The interaction between photochemical and biological processes in the degradation of marine dissolved organic matter (DOM) was investigated with seawater from a coastal southeastern U.S. salt marsh. Seawater supplemented with humic substances was exposed to alternating cycles of sunlight (equivalent to 8 h of midday sun) and dark incubations with natural bacterial populations (l-2 weeks in length). Photochemical degradation of the DOM was monitored during sunlight exposure by direct measurements of dissolved inorganic carbon (DIC) and carbon monoxide (CO) formation in 0.2-Frn filtered seawater. Bacterial degradation was monitored during dark incubations by tritiated leucine uptake and changes in bacterial numbers in bacterivore-free incubations and by direct measurements of DOM loss. The alternating cycles of sunlight and microbial activity resulted in more complete degradation of bulk DOM and marine humic substances than was found for nonirradiated controls (i.e. with microbial activity alone) by a factor of up to 3-fold. Increased decomposition was due both to direct losses of carbon gas photoproducts (DIC and CO in a 15 : 1 ratio) and to enhanced microbial degradation of photodegraded DOM, with approximately equal contributions from each pathway. Mass balance calculations indicated that low-molecular-weight carbon photoproducts, currently considered to be the compounds responsible for stimulating bacterial activity following photodegradation of DOM, were insufficient to account for the enhanced bacterial production observed. Thus, higher molecular weight, chemically uncharacterized fractions of DOM may also be modified to more biologically available forms during exposure to natural sunlight. Photochemical processes play a number of important roles in the biogeochemical cycling of dissolved organic matter (DOM) in natural waters. Water optical properties, biological processes, and trace element distributions have all been demonstrated to be affected, either directly or indirectly, by DOM photoreactions (Kieber et al. 1989; Blough and Zepp 1995; Siegel and Michaels 1996). Recently, the role of photochemical processes in the decomposition of DOM has received increasing recognition. Several studies have demonstrated that exposure to sunlight degrades larger molecules into smaller photoproducts that are removed from the DOM pool by two routes: through direct volatilization of carbon gases and through rapid microbial consumption of labile photoproducts (Kieber et al. 1990; Mopper et al. 1991; Miller and Zepp 1995; Wetzel et al. 1995; Graneli et al. 1996). The gaseous photoproducts of DOM are dominated by carbon monoxide (CO) and dissolved inorganic carbon (DIC). Photochemical formation of CO in surface waters has been studied for some time (Wilson et al. 1970; Conrad et al. 1982; Valentine and Zepp 1993), and concentrations of CO are known to reach 50 nM in the surface of freshwater Acknowledgments We thank Ed Sheppard and Wenying Ye for excellent technical assistance. Richard Zepp provided valuable suggestions and generous use of his laboratory equipment. Support for this project was provided by the NSF Land Margin Ecosystems Research Program (DEB 94-12089) and by a National Research Council postdoctoral award to W.L.M. systems on sunny days (Schmidt and Conrad 1993) and 6 nM in the open ocean (Conrad et al. 1982; Jones 1991). Recently, dissolved inorganic carbon (DIC) has also been identified as a direct photodegradation product of natural DOM (Miller and Zepp 1995; Salonen and Vahatalo 1994), with rates of photochemical formation high enough to partially explain the supersaturation of CO, commonly observed in surface freshwaters (Salonen and Vahatalo 1994; GranCli et al. 1996). Biologically available photoproducts of DOM include a number of low-molecular-weight compounds that can be readily assimilated by natural bacterial populations, including formic acid, formaldehyde, acetic acid, acetaldehyde, acetone, propanal, pyruvic acid, citric acid, levulinic acid, glyoxal, methylglyoxal, and glyoxylate (Mopper and Stahovec 1986; Kieber and Mopper 1987; Kieber et al. 1989, 1990; Mopper et al. 1991; Wetzel et al. 1995; Moran and Zepp 1997). Increased secondary production in microbial communities following exposure of natural DOM to sunlight has been well documented (Lindell et al. 1995; Wetzel et al. 1995; Geller 1986) and is presumably due to the assimilation of these low-molecular-weight carbon photoproducts. In addition, inorganic nitrogen has recently been identified among the suite of identified DOM photoproducts (Bushaw et al. 1996). Photochemical degradation of DOM is thus likely to have important effects on the biological productivity of many aquatic ecosystems limited by either carbon or nitrogen availability (Moran and Zepp 1997).