Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

Significance Coral reefs are highly productive ecosystems that raise a conundrum called “Darwin’s paradox”: How can high production flourish in low-nutrient conditions? We show here that in three abundant Caribbean sponges, the granules that have been commonly observed in sponge tissue for decades are polyphosphate granules. These granules can account for up to 40% of the total phosphorus (P) in sponge tissue. This finding has important implications for understanding P sequestration and recycling in the reef environment. We provide evidence that these granules are of bacterial origin and propose a P sequestration pathway by microbial symbionts and the sponge hosts. Considering the ancient origin of both partners, this process may have had an impact on the P cycle in Earth’s early history. Marine sponges are major habitat-forming organisms in coastal benthic communities and have an ancient origin in evolution history. Here, we report significant accumulation of polyphosphate (polyP) granules in three common sponge species of the Caribbean coral reef. The identity of the polyP granules was confirmed by energy-dispersive spectroscopy (EDS) and by the fluorescence properties of the granules. Microscopy images revealed that a large proportion of microbial cells associated with sponge hosts contained intracellular polyP granules. Cyanobacterial symbionts cultured from sponges were shown to accumulate polyP. We also amplified polyphosphate kinase (ppk) genes from sponge DNA and confirmed that the gene was expressed. Based on these findings, we propose here a potentially important phosphorus (P) sequestration pathway through symbiotic microorganisms of marine sponges. Considering the widespread sponge population and abundant microbial cells associated with them, this pathway is likely to have a significant impact on the P cycle in benthic ecosystems.