Testing the priming effect in the deep ocean: are microbes too starved to consume recalcitrant organic carbon?

ABSTRACT Deep ocean dissolved organic carbon (DOC) is one of the largest pools of reduced carbon on Earth. Many DOC compounds escape microbial degradation and persist for thousands of years in the ocean. Although many hypotheses have been proposed, the mechanisms responsible for this long-term stability remain unresolved. Heterotrophic microorganisms in the deep ocean are energetically starved and exhibit low metabolic activity. Here, we investigated whether the severe energy limitation in deep sea environments acts as a barrier to microbial degradation of DOC. We hypothesized that alleviating this energetic barrier through the addition of labile compounds (i.e., the priming effect) could stimulate microbial consumption of DOC. We conducted 62-day bottle incubations with deep seawater from the Southern Ocean that were amended with simple organic carbon, nitrogen- and/or phosphorus-containing compounds. We tracked DOC concentration, cell abundance and microbial community structure over the course of the experiment. Our results show no evidence of a priming effect regardless of the priming compound. However, priming compounds selected for distinct microbial populations with little overlap among amended bottles even when compounds were chemically similar. Pseudoalteromonas and Pseudomonas were enriched across all amended bottles, and their competition for labile substrates likely contributed to observed variations in DOC consumption. Our results reveal that the persistence of DOC is not driven by the energetic state of deep-sea microbes. In contrast, our results suggest that inputs of fresh carbon to the deep ocean are more likely to increase DOC sequestration, via the microbial carbon pump, rather than stimulate DOC consumption. IMPORTANCE The oceans store vast amounts dissolved organic carbon (DOC) that can resist microbial degradation for thousands of years. The mechanisms that underlie the long-term stability of DOC in the ocean are still debated. Microorganisms in this environment exhibit low metabolic activity and are energetically starved. We tested whether the microbial degradation of DOC could be stimulated through the addition of labile compounds. Surprisingly, alleviating energetic constraints did not stimulate the consumption of deep ocean DOC. Additionally, our results suggest that competition among taxa is an important constraint on dissolved organic carbon consumption, with implications for ecosystem processing. Our study indicates that an increase in fresh organic carbon to the deep ocean may enhance carbon sequestration since marine microbes are known to produce recalcitrant compounds. Among other applications, this finding is of consequence for ongoing geoengineering efforts that aim to remove atmospheric carbon by increasing carbon export to the deep sea.

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