Ultraviolet radiation blocks the organic carbon exchange between the dissolved phase and the gel phase in the ocean

Dissolved organic carbon (DOC) is one of the major reservoirs of active organic carbon on Earth. Although the bulk of the marine DOC pool is largely composed of small refractory polymeric material, new evidence suggests that ;10% of the DOC pool (1016 g C) can enter the microbial loop by forming microscopic gels that can eventually be colonized and degraded by bacteria. Marine microgels result from a spontaneous and reversible assembly/ dispersion equilibrium of DOC polymers forming hydrated Ca-bonded tangled polymer networks. Here we test the hypothesis that ultraviolet (UV) photocleavage should strongly inhibit the formation of microgels, because the stability of tangled networks decreases exponentially with polymer length. Because of the loss of ozone shielding, the UV-B spectral component of solar radiation (l 5 280–320 nm) has undergone a dramatic increase in the past few decades, particularly in the polar regions. We used dynamic laser-scattering spectroscopy and flow cytometry to investigate UV-induced DOC polymer cracking and the effect of UV on DOC assembly/dispersion equilibrium in 0.2 mm filtered seawater. Results indicate that exposure of seawater to UV-B fluxes equivalent to those found in Antarctica during summer solstice can cleave DOC polymers, inhibit their spontaneous assembly, and/or disperse assembled microgels. Our results agree with previous observations that indicated that fragmentation produced by UV photolysis increases exponentially with exposure time and suggested that UV could limit the supply of microbial substrate by hindering microgel formation. UV cleavage yields short-chain polymers that do not assemble and could eventually account for the old refractory DOC pool found in seawater. The ocean holds one of the largest stocks of organic carbon on earth, playing a major role in global biogeochemical carbon cycling (Druffel et al. 1992; Hedges 1992). However, the mechanisms of transformation and degradation of this massive carbon reservoir remain poorly understood (Kepkay 1994; Amon and Benner 1996; Benner 2002). The bioreactivity of marine organic carbon varies broadly. Regardless of their chemical nature, low-molecular-weight dissolved organic carbon (DOC; ,1,000 D) exhibits the lowest bioreactivity, whereas high-molecular-weight DOC and colloids support the bulk of marine heterotrophic microbial production (Kirchman et al. 1991; Kepkay 1994; Amon and Benner 1996). These features suggest that bioreactivity might be more dependent on quaternary conformation of larger molecules or on supramolecular association of smaller chains than on the presence of particular functional groups (Azam 1998; Azam and Long 2001). Recent observations lend strong support to the idea that an important fraction of the DOC pool is in dispersion/assembly equilibrium, forming 1 Corresponding author ([email protected]). Acknowledgments This work was supported by a grant from the Bioengineering Division of the US National Science Foundation under the Biocomplexity Program 0120579 to PV. We thank John Hedges, Karl Banse, Peter Jumars, Lee Karp-Boss, and Marc Wells for reading and commenting on early versions of the article. We also thank Tom Hinds, Evelyn Lessard, and Mary Jane Perry for the use of equipment, our reviewers, and particularly Mary Ann Moran for her patience and constructive criticism. supramolecular networks that might indeed play a critical role in bioreactivity (Chin et al. 1998; Wells 1998). Polymers present in the DOC fraction of seawater samples obtained from a broad range of sources can assemble spontaneously, forming the matrix of microscopic hydrogels (Fig. 1). These gels contain polysaccharide, lipid, protein, and nucleic acid chains and can range from colloidal size (100–200 nm) to 6–8 mm (Chin et al. 1998). DOC polymer assembly is reversible, exhibits the characteristic sigmoid time course of high-order kinetics, and at equilibrium has a thermodynamic yield of ;10% (Chin et al. 1998). If the studied seawaters are typical of the global DOC pool (7 3 1017 g C; Hedges 1992), then up to 7 3 1016 g C of organic carbon may occur in gel phase in the ocean. Within the scaling of the ‘‘sizerelated bioreactivity’’ of DOC (Kirchman et al. 1991; Amon and Benner 1996; Benner 2002), this huge mass of microgels and colloidal nanogels represents the biggest dimensional domain and the largest and most readily available pool of biodegradable organic carbon accessible to bacteria. Marine bacteria are known to readily degrade a large fraction of DOC produced by phytoplankton blooms (Kirchman et al. 1991). The advantage of gels as a microbial substrate can be explained because the ability of bacteria to cleave larger polymers into low-molecular-weight monomers—that can be rapidly incorporated and metabolized—relies on exoenzymes that are released by bacteria to the medium. The yield of the exoenzymes is higher when bacteria colonize polymer gel networks that contain a high concentration of substrate than when released to seawater that contains much lower 1619 UV-B blocks the assembly of DOC polymers Fig. 1. Dynamics of self-assembling polyanionic marine polymer gels (from Chin et al. 1998 and Wells 1998, with modifications). Hydrogels consist of a three-dimensional polymer network imbedded in water. Water prevents the collapse of the network, and the network entraps the water. Polyanionic polymer moieties found in the dissolved organic matter pool can spontaneously and reversibly assemble, forming nanometer-sized tangled networks that are stabilized by Ca21 bonds. The tangled nature of these nanogels allows polymers to interpenetrate neighboring gels, annealing into larger microgels. The size and stability of these gels depend on the charge density, hydrophobic/hydrophilic properties, length of the assembled polymers, and the kinematics of shear forces prevailing in seawater. The chemical and physical features of the individual polymer chains and the dielectric properties of the entrapped seawater determine the topological dynamics, the chemical and physical reactivity of the network, and how they interact with living organisms. Close intermolecular distances and hindered mobility produce a unique set of emergent properties that are different from those of the dispersed polymers that make up these networks. Polymer chains inside microgels are in a statistically stable neighborhood, creating microenvironments of high-substrate concentration that remain in thermodynamic equilibrium with the surrounding medium and serve as a rich source of substrate to microorganisms. concentrations of substrate (Azam 1998; Azam and Long 2001). Taken together, these ideas suggest that the marine gel phase derived from the assembly of DOC polymeric material must play a critical role in biogeochemical cycling (Wells 1998). Thus, events that interfere with DOC polymer assembly could potentially arrest the formation of microgels, blocking a critical route of microbial processing in the ocean. Here we show that high-energy ultraviolet (UV)–B light can readily cleave DOC polymers and effectively arrest the formation of microgels.