Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients

Abstract

Bacterioplankton respiration (BR) may represent the largest single sink of organic carbon in the biosphere and constitutes an important driver of atmospheric carbon dioxide (CO(2)) emissions from freshwaters. Complete understanding of BR is precluded by the fact that most studies need to assume a respiratory quotient (RQ; mole of CO(2) produced per mole of O(2) consumed) to calculate rates of BR. Many studies have, without clear support, assumed a fixed RQ around 1. Here we present 72 direct measurements of bacterioplankton RQ that we carried out in epilimnetic samples of 52 freshwater sites in Québec (Canada), using O(2) and CO(2) optic sensors. The RQs tended to converge around 1.2, but showed large variability (s.d.=0.45) and significant correlations with major gradients of ecosystem-level, substrate-level and bacterial community-level characteristics. Experiments with natural bacterioplankton using different single substrates suggested that RQ is intimately linked to the elemental composition of the respired compounds. RQs were on average low in net autotrophic systems, where bacteria likely were utilizing mainly reduced substrates, whereas we found evidence that the dominance of highly oxidized substrates, for example, organic acids formed by photo-chemical processes, led to high RQ in the more heterotrophic systems. Further, we suggest that BR contributes to a substantially larger share of freshwater CO(2) emissions than presently believed based on the assumption that RQ is ∼1. Our study demonstrates that bacterioplankton RQ is not only a practical aspect of BR determination, but also a major ecosystem state variable that provides unique information about aquatic ecosystem functioning.

Figure 1

Measured RQs during single-substrate bacterial bioassays plotted against theoretical RQ values for complete aerobic oxidation of the different substrates. Error bars show the range of values obtained by duplicate measurements. The theoretical RQs of the substrates are derived from Table 1, except tryptophan that is attributed the typical text book value of 0.8 for protein and amino-acid degradation. For complete incubation data, see Supplementary Figure S3.

Figure 2

Relationship between the rate of bacterial production of TCO₂ and the rate of bacterial consumption of dissolved oxygen (O₂) shown for different freshwater systems (n=110). Diagonally dashed lines represent different bacterial RQs. The figure compiles present (‘Lakes' and ‘Shallow ponds and tarns'), unpublished (‘Unpublished, rivers' M. Berggren unpublished^*) and previously published data (‘Literature, lakes' Cimbleris and Kalff (1998)^**). ^*Measured as in this study, but at a fixed temperature (20 °C) and controlled inorganic nutrient concentrations. ^**Measured during 2-day dark incubations at a controlled temperature of 21 °C using Winkler titration (O₂ consumption) and gas chromatography (TCO₂ production).

Figure 3

Relationships between the RQ of lake bacterioplankton (filled diamonds, n=51) and in situ (a) oxygen saturation, (b) pH and (c) partial pressure of CO₂. The RQ of bacterioplankton in shallow ponds and tarns (open diamonds, n=21) is shown is shown for comparison, although not being significantly correlated to any of the explanatory variables. (d) Box and whisker plots of all RQ observations grouped by system depth, area and CO₂ flux to air. Plus signs denote means and asterisks denote the significance of difference between means: ^**0.01, ^***0.001 (independent samples t-test). Note the logarithmized axes of (c).

Figure 4

PC loading plots, showing major axes (PCs) of variation in (a) ecosystem properties, (b) substrate quality and (c) bacterial community capacity to degrade different compounds on the Biolog Ecoplate. Percent explained variance by each PC is indicated in the axis title. Vectors show Pearson correlations between RQ and PC scores. Variables in italics have been log-transformed to improve normality. Asterisks and squares denote significant correlations with horizontal and vertical axis, respectively (single symbol P<0.05; double symbol P<0.01; triple symbol P<0.001).

Figure 5

Contribution of epilimnetic bacterial respiration (BR) to CO₂ efflux from different types of CO₂ supersaturated freshwaters. White bars show BR calculated from O₂ consumption assuming a fixed RQ of 1 and grey bars show BR measured directly as TCO₂ production. Bars show mean values and error bars denote 95% confidence intervals of the means (based on log values). Asterisks denote the significance of difference between paired log means: ^*0.05, ^**0.01, ^***0.001 (paired samples t-test).