A coupled phosphorus and carbon cycling mediated by prokaryotic microbes in the deepest trench

There has been a long-standing paradox in oceanic phosphorus (P) cycling in the ocean: high alkaline phosphatase activity (APA) persists in deep waters despite replete dissolved inorganic phosphorus (DIP), and active microbial regulatory mechanisms driving this pattern remain largely untested in the carbon-limited hadal zone. Here, we test the hypothesis that the observed elevated levels of deep-ocean APA is driven by microbial carbon demand, via full-depth water column analyses of dissolved organic phosphorus (DOP) and DIP in the Challenger Deep (Mariana Trench), combined with laboratory-based in situ-simulated high-pressure incubation experiments. We reveal two distinct phosphorus-alkaline phosphatase activity (P-APA) regulatory regimes: P-limitation-driven extreme APA in P-depleted surface waters, and sustained, elevated APA in P-replete, carbon-starved deep waters. Metabolically active alkaline phosphatase (AP)-producing taxa, most notably the SAR11 clade, were detectable throughout the full water column. Path analysis was used to evaluate the consistency of the observed data with a hypothesized causal framework linking active microbial communities, APA kinetics, and coupled phosphorus-carbon (P-C) cycling, with the model explaining 82.3% of the variance in dissolved organic carbon and 75.4% of the variance in DIP in the water column. We propose and validate a “piggyback” strategy whereby deep-sea microbes express AP to acquire carbon from DOP, offering a previously untested, potential mechanistic explanation for the long-standing deep APA paradox, while revealing a microbially mediated P-C coupling pathway that may represent a breakaway of deep-ocean carbon sequestration pathway.