Testing the priming effect in the deep ocean: are microorganisms 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. Interestingly, priming compounds were selected for distinct microbial populations even when the 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 suggest that the persistence of DOC is not driven by the energetic state of deep-sea microorganisms. These findings indicate that inputs of fresh carbon to the deep ocean are unlikely to trigger extensive degradation of the existing DOC pool, reinforcing its role as a stable long-term reservoir of carbon. IMPORTANCE The oceans store vast amounts of 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 suggests that the long-term stability of deep ocean DOC reflects inherent chemical or structural resistance to microbial degradation, rather than ecological or energetic constraints. This finding is also of consequence for ongoing geoengineering efforts that aim to remove atmospheric carbon by increasing carbon export to the deep sea.

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