Bacterial metabolism and growth efficiency in lakes: The importance of phosphorus availability

We investigated bacterial responses to variations in dissolved organic carbon (DOC) and nutrient availability by a comparative analysis of bacterial metabolism in lakes ranging from oligotrophic to eutrophic. Bacterial growth, respiration, and growth efficiency were quantified in lake water dilution cultures performed in 20 lakes located in eastern Quebec, Canada, which varied with respect to both DOC and nutrient concentrations. Intrinsic growth rates of the bacteria ranged from 0.1 to 1.4 d21, bacterial cell-specific respiration rates ranged from 0.4 to 7.2 fg C cell21 h21, and growth efficiencies ranged from 6.7% to 51.6%. These variations were unrelated to bulk DOC concentrations. Instead, growth rate and efficiency were positively related to total phosphorus concentrations. Specific respiration rate, on the other hand, decreased with increasing phosphorus concentrations, and the magnitude of respiration, on a per-cell basis, strongly influenced observed growth efficiencies. In a series of substrate enrichment experiments, additions of glucose alone failed to stimulate a response in growth rate, mean cell biovolume, or the potential biomass yield in dilution cultures, but all responded positively to phosphorus additions. Our results show that bacterial metabolism and the fate of DOC input to lake microbial communities are strongly dependent on phosphorus availability, rather than total carbon availability. Extreme oligotrophy appears to place high respiratory demands on the bacterioplankton, resulting in very low bacterial growth efficiencies and consequently greater DOC flow to CO2 than to biomass available for transfer to higher trophic levels. The organic carbon fueling bacterial metabolism in lakes originates from either in situ primary production (autochthonous carbon) or from terrestrial production that is carried into the lake from its watershed (allochthonous carbon). The relative importance of these two sources of carbon is highly variable among lakes. While autochthonous carbon tends to predominate in very eutrophic lakes, allochthonous carbon loading often greatly exceeds in situ primary production in oligotrophic lakes (Wetzel 1992). Input of allochthonous carbon thus represents a potentially large subsidy to the metabolism of lake communities. Several lines of evidence argue that the total respiratory breakdown of organic matter exceeds that produced by in situ primary production in most lakes (e.g., del Giorgio and Peters 1994; Cole et al. 2000). This metabolic imbalance (net heterotrophy; total respiration . gross primary production) implies that allochthonous carbon must support a portion of the lake’s total respiration. Indeed, it has recently been shown that, based on epilimnetic dissolved oxygen mea1 To whom correspondence should be addressed. Present address: Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208 ([email protected]).