Direct measurement of the d13C signature of carbon respired by bacteria in lakes: Linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes

Using a novel method to measure the isotopic signature (d13C) of respiratory CO2 produced by bacterioplankton, we determined the proportion of terrigenous vs. algal-derived organic carbon (OC) respired by bacteria in a series of eight lakes in southern Québec (Canada). The lakes are located within the same general basin but span a large range in trophic status, morphometry, and dissolved OC (DOC) concentrations. Isotopic d13C values of respired CO2 ranged from 228.4% to 232.5% across a gradient of lakes and streams. These values were compared with those of potential OC sources within the lakes (terrigenous and algal) using a mass balance model. The proportion of terrigenous OC respired varied from 3% to .70% and was strongly negatively correlated to lake chlorophyll a (Chl a) concentrations and weakly positively correlated to DOC : Chl a concentrations. While both total plankton and bacterial respiration (BR) increase with lake Chl a concentration, the component of BR that is supported by terrigenous OC, which ranges from 0.7 to 1.7 mg C L21 h21, stays essentially constant along the trophic gradient, increasing only slightly with DOC concentration. There is a relatively constant baseline BR supported by terrigenous OC, which becomes diluted by the BR of algal OC as the lakes become more productive. The estimated production of CO2 through BR of terrigenous OC in the epilimnion explains on average 60% of the estimated air–water CO2 flux calculated for these lakes, suggesting that the processing of allochthonous OC by bacteria is a major component of this flux. Lakes, and aquatic ecosystems in general, process organic carbon (OC) from a wide variety of sources. These sources may include carbon derived from internal primary production (e.g., phytoplankton, macrophytes) and external OC inputs from the surrounding wetlands and terrigenous ecosystems (Tranvik and Jansson 2002; Pace and Prairie 2005). Multiple lines of evidence suggest that a substantial proportion of these wetland and terrigenous inputs of OC is processed within lakes and rivers and fuels a variable but often significant portion of the total system respiration (del Giorgio et al. 1999; Cole et al. 2002; Pace and Prairie 2005). For example, the net heterotrophy that has been reported for many temperate and boreal lakes and reservoirs, where respiration exceeds gross primary production, can be achieved only if respiration is subsidized by the metabolism of OC derived from the catchment (del Giorgio et al. 1999; Cole et al. 2000). Organic carbon mass balances have further demonstrated that there is significant loss of terrigenous OC loaded into lakes, through a combination of sedimentation, photochemical degradation, and biological consumption (Molot and Dillon 1997; Tranvik and Jansson 2002; Algesten et al. 2004). More recently, whole lake 13C enrichments coupled with C cycling models have shown that a large fraction of total ecosystem respiration, of which most is bacterial, may be derived from allochthonous OC sources (Cole et al. 2002, 2007). The evidence that terrigenous OC is consumed in lakes and rivers is unequivocal, but because this evidence is derived primarily from indirect approaches (production : respiration measurements, carbon mass balances, air–water gas dynamics, isotope addition experiments, models), the proportion of total bacterial respiration (BR) in the water column of lakes and streams that is actually fueled by these external inputs remains to be empirically determined. Thus, although we know in general that (1) most lakes receive allochthonous organic inputs; (2) at least a portion of this terrigenous OC is respired, primarily by bacteria; and (3) the relative importance of this terrigenous OC supply to lake metabolism likely varies as a function of lake trophy, we still do not know the actual proportion of the various sources of OC that fuel BR in lakes at any given time, nor do we know how this proportion might vary over a seasonal cycle or across a gradient of lake and landscape types. Our inability to directly quantify the relative importance of the sources of OC respired by aquatic heterotrophic bacteria represents a major gap in our understanding of the physiological and environmental factors regulating C cycling across multiple time and space scales. At the ecosystem level, the processing and ultimate respiration of terrigenous OC influences multiple processes, 1 To whom correspondence should be addressed. Present address: Virginia Commonwealth University, Department of Biology, 1000 W. Cary Street, Richmond, Virginia 23284 ([email protected]). Acknowledgments We thank François Guillemette, Jérôme Comte, and Dominic Frechette for their tireless efforts in the field and lab and Catherine Beauchemin for her assistance with sample analyses. We are grateful to Gilles St-Jean and Paul Middlestead (Hatch Isotope Lab, University of Ottawa) for their invaluable advice, input, and expertise. We extend special thanks to Liz Canuel for assistance with lipid extractions, and to H. S. Canut for encouragement. The suggestions of three anonymous reviewers greatly improved the quality of this manuscript. This work was supported by grants from the National Science and Engineering Research Council of Canada and from the Fonds Québécois de la Recherché sur la Nature et les Technologies. Limnol. Oceanogr., 53(4), 2008, 1204–1216 E 2008, by the American Society of Limnology and Oceanography, Inc.