Copepod Grazing and Prokaryotic Decomposition Amplify the Effect of Diatom-Dinoflagellate Regime Change on Biological Carbon Pump Efficiency

Copepod fecal pellets (FPs) are an important but highly variable component of the global Biological Carbon Pump (BCP). This study decoupled and quantified how copepod grazing and prokaryotic activities affect BCP efficiency under different phytoplankton dietary regimes. With a diet of diatoms, copepod FP production rates double, FP sinking rates triple, and FP decomposition rates are significantly lower relative to those with dinoflagellate diets. When dinoflagellates are the primary producers, inefficient grazing and enhanced prokaryotic activity synergistically decrease the efficiency of FP exports to the deep ocean. This finding confirms previous observations. Opportunistic particle-attached (PA) prokaryotes are crucial for FP decomposition. Metagenomic analyses revealed that CAZymes and lysosomal enzyme abundances highly correlated with FP decomposition rates, representing important bioindicators of FP decomposition. These functional enzymes targeting phytoplankton- and copepod-intestine-derived macromolecules from the PA prokaryotic communities were key to FP decomposition. Genomic properties of the Planctomycetota revealed that strong motile ability, detoxification systems, and macromolecule degradation enzymes enabled the success of these opportunistic PA prokaryotes. Elevated temperatures amplified FP decomposition rates by enhancing enzyme abundances and especially accelerated the decomposition of FPs composed of dinoflagellates. This reduced BCP efficiency, as rapidly recycled organic materials remain in surface waters. Our findings highlight the synergistic biological activities amplifying the effects of phytoplankton composition changes on BCP efficiency. This underscores the importance of considering grazing regimes in combination with microbial dynamics in assessing ocean carbon cycling.