The role of organic acid exudates in liberating phosphorus from seagrass-vegetated carbonate sediments

Sediment-bound phosphorus (P) is a potential nutrient source for P-limited seagrasses inhabiting carbonate sediments. We explored the role of organic acid (OA) exudation by seagrasses in liberating mineral P from carbonate sediments. Organic acids can act to increase available P by dissolving carbonate sediment, competing with P for binding sites and complexing dissolution end products, and also by fueling microbial processes that change pore-water pH. We used dialysis tubing placed around individual roots in situ to quantify dissolved species immediately adjacent to roots (root zone) and compared these to bulk pore-water concentrations in vegetated and nonvegetated sediments. Total OA concentrations were highest in the root zone (29.8 6 1.8 mmol L21) compared to bulk measures of 15.5 6 1.9 and 7.5 6 0.6 mmol L21 in vegetated and nonvegetated sediments, respectively. Phosphate concentrations were also highest in the root zone and were linearly related to OA concentrations (R2 5 0.63). Organic acid concentrations increased along a seagrass productivity gradient, and ratios of OA concentrations to productivity showed a significant response to a gradient in P-limitation of seagrasses. Organic acid concentrations found in and around roots, compared to those found in bulk sediment measures, indicate that seagrasses are a significant source of OA. Sampling at small spatial scales (mm) immediately adjacent to the roots is critical, because bulk sediment pore-water measures did not capture the observed fluctuations caused by the rapid reaction and consumption of OA in the sediment. Root-zone processes can liberate considerable quantities of P, and OA exudates likely contribute significantly to the success of T. testudinum in P-limited environments. Organic acid exudation from seagrass roots has the potential to liberate phosphorus (P) from carbonate marine sediments that are characteristic of many subtropical and tropical environments. Since organic acid (OA) exudates from terrestrial plant roots have been shown to increase the dissolution of phosphate (Pi) rocks (Ryan et al. 2001; Strom et al. 2002; Jones et al. 2003) it is hypothesized that seagrasses may exhibit an analogous mechanism. However, there have been no attempts to address the dissolution of carbonate sediments by OA exudates in marine environments and the potential of this process to make mineral Pi available to P-limited seagrasses. Organic acids are here defined as low-molecular-weight organic compounds that contain at least one carboxyl group and are not amino acids. The conceptual diagram in Fig. 1 illustrates the simplified biotic and abiotic mechanisms by which OA exudates, along with O2 release, may influence Pi availability in marine carbonate sediments surrounding seagrass root tips. Organic acids can react abiotically with carbonate sediment minerals and solubilize Pi through a number of mechanisms. First, the organic anion may displace Pi on adsorption sites on minerals and organic matter or decrease the total amount of adsorption sites available (Jones 1998; Ryan et al. 2001; Strom et al. 2001). Second, the organic anion may chelate metal and carbonate dissolution end products, such as Ca2+ ions, that would otherwise immobilize Pi (Knight et al. 1992; Kirk 1999; Strom et al. 2001). Third, if the excretion of the organic anion is accompanied by the excretion of protons (H+) or if it is released as an acid, a localized decrease in pH will be observed around the root surface and the dissolution of carbonate minerals will release Pi (Bolan et al. 1997; Kirk 1999; Jones et al. 2003). The consumption of OA by microbes also likely contributes to carbonate sediment dissolution through the production of aqueous CO2 and H+. The aerobic respiration of sediment organic matter (which may include OA) results in the production of aqueous CO2, which lowers the saturation state of carbonate minerals in sediment pore waters (Burdige and Zimmerman 2002; Hu and Burdige 2007). Organic acids may also be consumed through fermentation and sulfate reduction, by which CO2 and end products such as ethanol, acetic, and lactic acids are produced. Sulfate reduction results in the net production of acidity due to the tight coupling between sulfide oxidation and sulfate reduction, which is balanced by diel fluctuations in seagrass O2 release (Ku et al. 1999; Burdige and Zimmerman 2002; Hu and Burdige 2007). The mechanisms of OA exudation are largely unknown and their contribution to sediment dissolution depends on how and in what magnitude they are metabolized by microbes as well as whether they are released as anions or acids (Strom et al. 2002; Jones et al. 2003). In terrestrial sediments, the reaction of organic anions with carbonate minerals has been shown to increase Pi concentrations and sediment dissolution, even though the anions do not directly increase acidity (Kirk 1999; Ryan et al. 2001). This is due to multivalent OA, which have the most significant effect on Pi availability because they compete 1Corresponding author ([email protected]). Acknowledgments This research was funded by the University of Virginia and the Jones Everglades Research Fund. Special thanks to Amie Aguiar, Thomas Frankovich, Renee Gruber, Bret Wolfe, and Eric Bricker for assistance in field and laboratory work. Limnol. Oceanogr., 53(6), 2008, 2616–2626 E 2008, by the American Society of Limnology and Oceanography, Inc.