The influence of dissolved organic carbon on bacterial phosphorus uptake and bacteria– phytoplankton dynamics in two Minnesota lakes

The balance of production in any ecosystem is dependent on the flow of limiting nutrients into either the autotrophic or heterotrophic components of the food web. To understand one of the important controls on the flow of inorganic nutrients between phytoplankton and bacterioplankton in lakes, we manipulated dissolved organic carbon (DOC) in two lakes of different trophic status. We hypothesized that labile DOC additions would increase bacterial phosphorus (P) uptake and decrease the response of phytoplankton to nutrient additions. Supplemental nutrients and carbon (C), nitrogen (N, 1.6 mmol NH4Cl L21 d21), P (0.1 mmol KH2PO4 L21 d21), and DOC (glucose, 15 mmol C L21 d21) were added twice daily to 8-liter experimental units. We tested the effect of added DOC on chlorophyll concentration, bacterial production, biomass, and P uptake using size-fractionated P-PO4 uptake. In the oligotrophic lake, DOC additions stimulated bacterial production and increased bacterial biomass-specific P uptake. Bacteria consumed added DOC, and chlorophyll concentrations were significantly lower in carboys receiving DOC additions. In the eutrophic lake, DOC additions had less of a stimulatory effect on bacterial production and biomass-specific P uptake. DOC accumulated over the time period, and there was little evidence for a DOC-induced decrease in phytoplankton biomass. Bacterial growth approached the calculated mmax and yet did not accumulate biomass, indicating significant biomass losses, which may have constrained bacterial DOC consumption. Excess bacterial DOC consumption in oligotrophic lakes may result in greater bacterial P affinity and enhanced nutrient uptake by the heterotrophic compartment of the food web. On the other hand, constraints on bacterial biomass accumulation in eutrophic lakes, from either viral lysis or bacterial grazing, can allow labile DOC to accumulate, thereby negating the effect of excess DOC on the planktonic food web. Dissolved organic carbon (DOC) influences the physical, chemical, and biological characteristics of aquatic habitats (Wetzel 1992). DOC inputs can affect overall lake metabolism by either reducing light availability to autotrophs, as is the case in humic lakes (Carpenter et al. 1998; Kankaala et al. 1996), or by stimulating bacterial growth, as is demonstrated by whole-lake DOC additions (Blomqvist et al. 2001). Relief from carbon limitation presumably makes heterotrophic bacteria more competitive for other nutrients, such as phosphorus (P), which are often limiting to phytoplankton primary production as well. Heterotrophic bacteria have a greater affinity for phosphorus than phytoplankton (Currie and Kalff 1984; Cotner and Wetzel 1992; Jansson 1993) and can outcompete phytoplankton for phosphorus at low nutrient concentrations (Rhee 1972; Jansson 1993). The failure of bacteria to displace phytoplankton in P-limited aquatic ecosystems was initially attributed to bacterial DOC limitation (Currie and Kalff 1984). However, inorganic nutrients limit bacterial production in a variety of aquatic habitats (Cotner et al. 1997; Thingstad et al. 1998; Caron et al. 2000), casting doubt on the universality of bacterial DOC limitation. There is a growing recognition of the importance of food-web structure, including grazer control of bacterial metabolism (Thingstad et al. 1997) and the ability of some planktonic autotrophs to compete with bacteria for inorganic nutrients (Havskum et al. 2003). Additionally, the finding that bacteria can be simultaneously limited by more than one substrate (Rivkin and Andersen 1997) suggests that traditional resource competition theory does not adequately describe bacterial nutrient requirements. Microbiological studies provide evidence of a biochemical link between DOC metabolism and bacterial inorganic nutrient uptake. Some high-affinity nutrient-uptake systems are energetically expensive and require excess DOC metabolism to become fully operational (Teixeira de Mattos and Neijssel 1997). Jansson (1993) found that the high-affinity phosphorus uptake system in Pseudomonas only functioned in the presence of excess glucose. According to this evidence, DOC additions would not only drive bacteria toward inorganic nutrient limitation, but would enhance bacterial nutrient affinity. Despite the evidence for a link between DOC metabolism and bacterial nutrient uptake, the ecological significance of these findings is not clear. Published studies lack consensus on whether DOC additions encourage bacterial dominance in aquatic ecosystems. Several studies confirm the prediction that DOC additions will cause a coincident increase in bacterial biomass and decrease in phytoplank1 Corresponding author ([email protected]). Present address: U.S. Geological Survey, 3215 Marine Street, Suite E-127, Boulder, Colorado 80303. Acknowledgments We thank J. Finlay, R. Sterner, and M. Pace, as well as two anonymous reviewers, for their constructive comments and assistance in improving the manuscript. Financial support for this experiment was provided by the University of Minnesota Dayton and Wilkie Natural History Fund. Limnol. Oceanogr., 53(1), 2008, 137–147 E 2008, by the American Society of Limnology and Oceanography, Inc.