Abstract
Respiratory and catabolic genes are differentially distributed across microbial genomes. Thus, specific carbon sources may favor different respiratory processes. We profiled the influence of 94 carbon sources on the end products of nitrate respiration in microbial enrichment cultures from diverse terrestrial environments. We found that some carbon sources consistently favor dissimilatory nitrate reduction to ammonium (DNRA/nitrate ammonification) while other carbon sources favor nitrite accumulation or denitrification. For an enrichment culture from aquatic sediment, we sequenced the genomes of the most abundant strains, matched these genomes to 16S rDNA exact sequence variants (ESVs), and used 16S rDNA amplicon sequencing to track the differential enrichment of functionally distinct ESVs on different carbon sources. We found that changes in the abundances of strains with different genetic potentials for nitrite accumulation, DNRA or denitrification were correlated with the nitrite or ammonium concentrations in the enrichment cultures recovered on different carbon sources. Specifically, we found that either L-sorbose or D-cellobiose enriched for a Klebsiella nitrite accumulator, other sugars enriched for an Escherichia nitrate ammonifier, and citrate or formate enriched for a Pseudomonas denitrifier and a Sulfurospirillum nitrate ammonifier. Our results add important nuance to the current paradigm that higher concentrations of carbon will always favor DNRA over denitrification or nitrite accumulation, and we propose that, in some cases, carbon composition can be as important as carbon concentration in determining nitrate respiratory end products. Furthermore, our approach can be extended to other environments and metabolisms to characterize how selective parameters influence microbial community composition, gene content, and function.
Highlights
Heterotrophic nitrate respiration is a critical juncture in the nitrogen and carbon cycles
While thermodynamic calculations predict that higher concentrations of electron donor will favor DNRA over denitrification [5], the specific carbon source available to drive DNRA must be utilized by the DNRA-capable subpopulations in Selective carbon sources influence the end products of microbial nitrate respiration the system
We postulate that certain, selective carbon sources are more likely to drive microbial nitrate respiration toward specific end products such as dinitrogen (N2), ammonium (NH4+), or intermediate nitrogen oxides (NO2−, NO, N2O), especially in systems with less complex microbial communities in which it is more likely that a given carbon catabolic trait is exclusively associated with a microbial subpopulation with a limited set of respiratory traits
Summary
Heterotrophic nitrate respiration is a critical juncture in the nitrogen and carbon cycles. While thermodynamic calculations predict that higher concentrations of electron donor will favor DNRA over denitrification [5], the specific carbon source available to drive DNRA must be utilized by the DNRA-capable subpopulations in Selective carbon sources influence the end products of microbial nitrate respiration the system. We postulate that certain, selective carbon sources are more likely to drive microbial nitrate respiration toward specific end products such as dinitrogen (N2), ammonium (NH4+), or intermediate nitrogen oxides (NO2−, NO, N2O), especially in systems with less complex microbial communities in which it is more likely that a given carbon catabolic trait is exclusively associated with a microbial subpopulation with a limited set of respiratory traits
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