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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.

Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus populations in separate ocean basins often mirrors the selective pressures imposed by the region's distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, particularly at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of Prochlorococcus.

Intraspecific trait variability has important consequences for the function and stability of marine ecosystems. Here we examine variation in the ability to use nitrate across hundreds of Prochlorococcus genomes to better understand the modes of evolution influencing intraspecific allocation of ecologically important functions. Nitrate assimilation genes are absent in basal lineages but occur at an intermediate frequency that is randomly distributed within recently emerged clades. The distribution of nitrate assimilation genes within clades appears largely governed by vertical inheritance, gene loss, and homologous recombination. By mapping this process onto a model of Prochlorococcus’ macroevolution, we propose that niche-constructing adaptive radiations and subsequent niche partitioning set the stage for loss of nitrate assimilation genes from basal lineages as they specialized to lower light levels. Retention of these genes in recently emerged lineages has likely been facilitated by selection as they sequentially partitioned into niches where nitrate assimilation conferred a fitness benefit.

Utilization of nitrate as a nitrogen source is broadly conserved among marine phytoplankton, yet many strains of Prochlorococcus lack this trait. Among cultured strains, nitrate assimilation has only been observed within two clades of Prochlorococcus: the high-light adapted HLII clade and the low-light adapted LLI clade. To better understand the frequency and dynamics of nitrate assimilation potential among wild Prochlorococcus, we measured seasonal changes in the abundance of cells containing the nitrate reductase gene (narB) in the subtropical North Atlantic and North Pacific oceans. At the Atlantic station, the proportion of HLII cells containing narB varied with season, with the highest frequency observed in stratified waters during the late summer, when inorganic nitrogen concentrations were lowest. The Pacific station, with more persistent stratification and lower N : P ratios, supported a perennially stable subpopulation of HLII cells containing narB. Approximately 20–50% of HLII cells possessed narB under stratified conditions at both sites. Since HLII cells dominate the total Prochlorococcus population in both ecosystems, nitrate potentially supports a significant fraction of the Prochlorococcus biomass in these waters. The abundance of LLI cells containing narB was positively correlated with nitrite concentrations at the Atlantic station. These data suggest that Prochlorococcus may contribute to the formation of primary nitrite maxima through incomplete nitrate reduction and highlight the potential for interactions between Prochlorococcus and sympatric nitrifying microorganisms. Further examination of these relationships will help clarify the selection pressures shaping nitrate utilization potential in low-light and high-light adapted Prochlorococcus.

The marine cyanobacterium Prochlorococcus is the smallest and most abundant photosynthetic organism on Earth. In this Review, we summarize our understanding of the diversity of this remarkable phototroph and describe its role in ocean ecosystems. We discuss the importance of interactions of Prochlorococcus with the physical environment, with phages and with heterotrophs in shaping the ecology and evolution of this group. In light of recent studies, we have come to view Prochlorococcus as a 'federation' of diverse cells that sustains its broad distribution, stability and abundance in the oceans via extensive genomic and phenotypic diversity. Thus, it is proving to be a useful model system for elucidating the forces that shape microbial populations and ecosystems., Gordon and Betty Moore Foundation (Grant GBMF495), National Science Foundation (U.S.) (Grant OCE-1153588), National Science Foundation (U.S.) (Grant OCE-1356460), National Science Foundation (U.S.) (Grant DBI-0424599), Center for Microbial Oceanography: Research and Education

The discovery of ammonia oxidation by mesophilic and thermophilic Crenarchaeota and the widespread distribution of these organisms in marine and terrestrial environments indicated an important role for them in the global nitrogen cycle. However, very little is known about their physiology or their contribution to nitrification. Here we report oligotrophic ammonia oxidation kinetics and cellular characteristics of the mesophilic crenarchaeon 'Candidatus Nitrosopumilus maritimus' strain SCM1. Unlike characterized ammonia-oxidizing bacteria, SCM1 is adapted to life under extreme nutrient limitation, sustaining high specific oxidation rates at ammonium concentrations found in open oceans. Its half-saturation constant (K(m) = 133 nM total ammonium) and substrate threshold (

The marine cyanobacterium Prochlorococcus is the most abundant photosynthetic organism in oligotrophic regions of the oceans. The inability to assimilate nitrate is considered an important factor underlying the distribution of Prochlorococcus , and thought to explain, in part, low abundance of Prochlorococcus in coastal, temperate, and upwelling zones. Here, we describe the widespread occurrence of a genomic island containing nitrite and nitrate assimilation genes in uncultured Prochlorococcus cells from marine surface waters. These genes are characterized by low GC content, form a separate phylogenetic clade most closely related to marine Synechococcus , and are located in a different genomic region compared with an orthologous cluster found in marine Synechococcus strains. This sequence distinction suggests that these genes were not transferred recently from Synechococcus . We demonstrate that the nitrogen assimilation genes encode functional proteins and are expressed in the ocean. Also, we find that their relative occurrence is higher in the Caribbean Sea and Indian Ocean compared with the Sargasso Sea and Eastern Pacific Ocean, which may be related to the nitrogen availability in each region. Our data suggest that the ability to assimilate nitrite and nitrate is associated with microdiverse lineages within high- and low-light (LL) adapted Prochlorococcus ecotypes. It challenges 2 long-held assumptions that ( i ) Prochlorococcus cannot assimilate nitrate, and ( ii ) only LL adapted ecotypes can use nitrite. The potential for previously unrecognized productivity by Prochlorococcus in the presence of oxidized nitrogen species has implications for understanding the biogeography of Prochlorococcus and its role in the oceanic carbon and nitrogen cycles.

The marine cyanobacterium Prochlorococcus is the numerically dominant photosynthetic organism in the oligotrophic oceans, and a model system in marine microbial ecology. Here we report 27 new whole genome sequences (2 complete and closed; 25 of draft quality) of cultured isolates, representing five major phylogenetic clades of Prochlorococcus. The sequenced strains were isolated from diverse regions of the oceans, facilitating studies of the drivers of microbial diversity—both in the lab and in the field. To improve the utility of these genomes for comparative genomics, we also define pre-computed clusters of orthologous groups of proteins (COGs), indicating how genes are distributed among these and other publicly available Prochlorococcus genomes. These data represent a significant expansion of Prochlorococcus reference genomes that are useful for numerous applications in microbial ecology, evolution and oceanography., Gordon and Betty Moore Foundation (Grant GBMR #495.01), National Science Foundation (U.S.) (Grant OCE-1153588), National Science Foundation (U.S.) (Grant OCE-0425602), National Science Foundation (U.S.) (Grant DBI-0424599), Center for Microbial Oceanography: Research and Education

Production of dissolved organic matter (DOM) by marine phytoplankton supplies the majority of organic substrate consumed by heterotrophic bacterioplankton in the sea. This production and subsequent consumption converts a vast quantity of carbon, nitrogen and phosphorus between organic and inorganic forms, directly impacting global cycles of these biologically important elements. Details regarding the chemical composition of DOM produced by marine phytoplankton are sparse, and while often assumed, it is not currently known if phylogenetically distinct groups of marine phytoplankton release characteristic suites of DOM. To investigate the relationship between specific phytoplankton groups and the DOM they release, hydrophobic phytoplankton-derived dissolved organic matter (DOMP) from eight axenic strains was analyzed using high-performance liquid chromatography coupled to mass spectrometry (HPLC-MS). Identification of DOM features derived from Prochlorococcus, Synechococcus, Thalassiosira and Phaeodactylum revealed DOMP to be complex and highly strain dependent. Connections between DOMP features and the phylogenetic relatedness of these strains were identified on multiple levels of phylogenetic distance, suggesting that marine phytoplankton produce DOM that in part reflects its phylogenetic origin. Chemical information regarding the size and polarity ranges of features from defined biological sources was also obtained. Our findings reveal DOMP composition to be partially conserved among related phytoplankton species, and implicate marine DOM as a potential factor influencing microbial diversity in the sea by acting as a link between autotrophic and heterotrophic microbial community structures.