Sponge symbionts and the marine P cycle.

Marine sponges are ubiquitous colonizers of shallow, clear-water environments in the oceans (1, 2). Sponges have emerged as significant mediators of biogeochemical fluxes in coastal zones by virtue of respiring organic matter and facilitating both the consumption and release of nutrients (3, 4). Sponges gain their nutrition through filtering out plankton and organic detritus and through uptake of dissolved organic matter from seawater (4). Many species host diverse microbial symbiont communities that contribute to digestion and nutrient release from the filtered organics, and in some species cyanobacterial symbionts can supply fresh photosynthate to meet a substantial fraction of the sponge energy requirements (5). In PNAS, Zhang et al. (6) reveal a major and heretofore unknown role for sponges with regard to the marine phosphorus cycle. The authors present strong evidence for polyphosphate (poly-P) production and storage by sponge endosymbionts. Zhang et al. also may have detected apatite, a calcium phosphate mineral, in sponge tissue. This work has major implications for our understanding of nutrient cycling in reef environments, the roles played by microbial endosymbiont communities in general, and aspects of P cycling on geologic timescales. Reef ecosystems harbor some of the greatest concentrations of biodiversity in the marine environment (7). This diversity is supported in part by gross rates of photosynthesis that can approach those of tropical rainforests (8, 9). However, reefs persist in extremely low nutrient environments and show little net production of organic matter. Sponges have proven to be key players in facilitating this rapid treadmill of photosynthetic and respiratory turnover of carbon (4). Sponges are major biogeochemical agents by virtue of their abundance coupled with the large volumes of water they process (Fig. 1), many species in excess of 10,000 body volumes of seawater per day (11, 12). Sponges metabolize a significant fraction of reef primary production (4) and also return organic carbon to the reef environment through shedding of cellular materials, which are rapidly consumed by detritivores (13). Sponges mediate a complex array of nutrient transformations. The net effect is to release labile nutrient forms (nitrate, nitrite, ammonium, phosphate) from less bioavailable organic molecules (3, 4, 14). Sponge endosymbionts also supply and remove fixed N to the reef ecosystem via N fixation (15) and denitrification and anaerobic ammonia oxidation (annamox) (4). Very few studies have determined the change in concentration of dissolved and particulate P between ambient waters and sponge effluent (Fig. 2). These studies show a net release of dissolved inorganic P in the form of orthophosphate (Pi) (4). However, the change in concentrations of particulate and dissolved organic P (Δ[POP] and Δ[DOP], respectively) are rarely measured in water passing through sponges. The change in C:N:P stoichiometry between sponge inputs and outputs will influence nutrient limitation in reef environments. However, endosymbiont photosynthesis, N fixation, denitrification, and annamox all complicate this determination. Now poly-P accumulation poses another challenge to the study of the ecological stoichiometry of sponges. Zhang et al. (6) present several lines of evidence that sponge endosymbionts accumulate P in the form of poly-P granules. These lines of evidence include fluorescence microscopy, whole-tissue poly-P extraction, scanning electron microscope-energy dispersive spectroscopy compositional analysis of granules, and detection of genes and gene transcripts for poly-P kinase, an enzyme responsible for bacterial poly-P synthesis. In the three sponge species examined, poly-P constitutes 25–40% of the total P in sponge tissue. The accumulation of abundant poly-P granules begs the question, “To what end?” The phosphoanhydride bonds that form the backbone of poly-P are analogous to those in ATP and might be used for energy storage, among other biochemical and regulatory