No abstract

Significance Phosphonates are a class of phosphorus metabolites characterized by a highly stable C-P bond. Phosphonates accumulate to high concentrations in seawater, fuel a large fraction of marine methane production, and serve as a source of phosphorus to microbes inhabiting nutrient-limited regions of the oligotrophic ocean. Here, we show that 15% of all bacterioplankton in the surface ocean have genes phosphonate synthesis and that most belong to the abundant groups Prochlorococcus and SAR11. Genomic and chemical evidence suggests that phosphonates are incorporated into cell-surface phosphonoglycoproteins that may act to mitigate cell mortality by grazing and viral lysis. These results underscore the large global biogeochemical impact of relatively rare but highly expressed traits in numerically abundant groups of marine bacteria.

Approximately 30% of the ocean's surface is subject to phytoplankton iron (Fe) limitation, especially in the Equatorial Pacific and Southern Oceans where upwelling provides a large flux of nitrate (NO 3 − ) and other nutrients (Moore et al., 2001(Moore et al., , 2013. Elsewhere, stratification of the upper ocean leads to depletion of NO 3 − , ammonia, and other bioavailable forms of nitrogen. In stratified oligotrophic gyres, shallow mixed layers also act to concentrate Fe deposited at the ocean's surface by atmospheric sources (Boyle et al., 2005;Sedwick et al., 2005). The large flux of Fe relative to NO 3 − in these ecosystems results in nitrogen limitation of photosynthesis and selects for phytoplankton like the cyanobacterium Prochlorococcus (Ward et al., 2013;Wu et al., 2000), whose small size allows them to outcompete other phytoplankton for recycled nitrogen species found at nanomolar concentrations (Morel et al., 1991).However, the same stratification that leads to Fe-rich conditions in the surface ocean can also impede Fe supply to the subsurface. Shallow mixed layers ensure that Fe derived from dust deposition does not reach the entirety of the euphotic zone, which can extend below 100 m in subtropical gyres. Stratification also limits the supply of regenerated Fe from below the euphotic zone. Indeed, a common feature of dFe profiles within subtropical gyres is a concentration minimum between 75 and 150 m (Bruland et al., 1994;Fitzsimmons et al., 2015;Sedwick et al., 2005). This subsurface dFe minimum often coincides with the deep chlorophyll maximum (DCM), a unique habitat where low irradiance drives phytoplankton photo-acclimation, increasing chlorophyll per cell to improve photosynthetic light capture (Letelier et al., 2004). Theoretical arguments suggest the increases in chlorophyll per cell should be matched by an equivalent increase in the number of Fe-bearing photosynthetic reaction

Phosphonates, organic compounds with a C-P bond, constitute 20-25% of phosphorus in high molecular weight dissolved organic matter and are a significant phosphorus source for marine microbes. However, little is known about phosphonate sources, biological function, or biogeochemical cycling. Here, we determine the biogeographic distribution and prevalence of phosphonate biosynthesis potential using thousands of genomes and metagenomes from the upper 250 meters of the global ocean. Potential phosphonate producers are taxonomically diverse, occur in widely distributed and abundant marine lineages (including SAR11 and Prochlorococcus) and their abundance increases with depth. Within those lineages, phosphonate biosynthesis and catabolism pathways are mutually exclusive, indicating functional niche partitioning of organic phosphorus cycling in the marine microbiome. Surprisingly, one strain of Prochlorococcus (SB) can allocate more than 40% of its cellular P-quota towards phosphonate production. Chemical analyses and genomic evidence suggest that phosphonates in this strain are incorporated into surface layer glycoproteins that may act to reduce mortality from grazing or viral infection. Although phosphonate production is a low-frequency trait in Prochlorococcus populations (~ 5% of genomes), experimentally derived production rates suggest that Prochlorococcus could produce a significant fraction of the total phosphonate in the oligotrophic surface ocean. These results underscore the global biogeochemical impact of even relatively rare functional traits in abundant groups like Prochlorococcus and SAR11.

Approximately 30% of the ocean's surface is subject to phytoplankton iron (Fe) limitation, especially in the Equatorial Pacific and Southern Oceans where upwelling provides a large flux of nitrate (NO 3 − ) and other nutrients (Moore et al., 2001(Moore et al., , 2013. Elsewhere, stratification of the upper ocean leads to depletion of NO 3 − , ammonia, and other bioavailable forms of nitrogen. In stratified oligotrophic gyres, shallow mixed layers also act to concentrate Fe deposited at the ocean's surface by atmospheric sources (Boyle et al., 2005;Sedwick et al., 2005). The large flux of Fe relative to NO 3 − in these ecosystems results in nitrogen limitation of photosynthesis and selects for phytoplankton like the cyanobacterium Prochlorococcus (Ward et al., 2013;Wu et al., 2000), whose small size allows them to outcompete other phytoplankton for recycled nitrogen species found at nanomolar concentrations (Morel et al., 1991).However, the same stratification that leads to Fe-rich conditions in the surface ocean can also impede Fe supply to the subsurface. Shallow mixed layers ensure that Fe derived from dust deposition does not reach the entirety of the euphotic zone, which can extend below 100 m in subtropical gyres. Stratification also limits the supply of regenerated Fe from below the euphotic zone. Indeed, a common feature of dFe profiles within subtropical gyres is a concentration minimum between 75 and 150 m (Bruland et al., 1994;Fitzsimmons et al., 2015;Sedwick et al., 2005). This subsurface dFe minimum often coincides with the deep chlorophyll maximum (DCM), a unique habitat where low irradiance drives phytoplankton photo-acclimation, increasing chlorophyll per cell to improve photosynthetic light capture (Letelier et al., 2004). Theoretical arguments suggest the increases in chlorophyll per cell should be matched by an equivalent increase in the number of Fe-bearing photosynthetic reaction