Metagenomic analysis reveals global-scale patterns of ocean nutrient limitation.

Nutrient supply regulates the activity of phytoplankton, but the global biogeography of nutrient limitation and co-limitation is poorly understood. Prochlorococcus adapt to local environments by gene gains and losses, and we used genomic changes as an indicator of adaptation to nutrient stress. We collected metagenomes from all major ocean regions as part of the Global Ocean Ship-based Hydrographic Investigations Program (Bio-GO-SHIP) and quantified shifts in genes involved in nitrogen, phosphorus, and iron assimilation. We found regional transitions in stress type and severity as well as widespread co-stress. Prochlorococcus stress genes, bottle experiments, and Earth system model predictions were correlated. We propose that the biogeography of multinutrient stress is stoichiometrically linked by controls on nitrogen fixation. Our omics-based description of phytoplankton resource use provides a nuanced and highly resolved description of nutrient stress in the global ocean.

Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus†MED4 I: uptake physiology.

Recent measurements of natural populations of the marine cyanobacterium Prochlorococcus indicate this numerically dominant phototroph assimilates phosphorus (P) at significant rates in P-limited oceanic regions. To better understand uptake capabilities of Prochlorococcus under different P stress conditions, uptake kinetic experiments were performed on Prochlorococcus MED4 grown in P-limited chemostats and batch cultures. Our results indicate that MED4 has a small cell-specific Vmax but a high specific affinity (αP ) for P, making it competitive with other marine cyanobacteria at low P concentrations. Additionally, MED4 regulates its uptake kinetics in response to P stress by significantly increasing Vmax and αP for both inorganic and organic P (PO4 and ATP). The Michaelis-Menten constant, KM , for PO4 remained constant under different P stress conditions, whereas the KM for ATP was higher when cells were stressed for PO4 , pointing to additional processes involved in uptake of ATP. MED4 cleaves the PO4 moieties from ATP, likely with a 5'-nucleotidase-like enzyme rather than alkaline phosphatase. MED4 exhibited distinct physiological differences between cells under steady-state P limitation versus those transitioning from P-replete to P-starved conditions. Thus, MED4 employs a variety of strategies to deal with changing P sources in the oceans and displays complexity in P stress acclimation and regulatory mechanisms.

The origins of cooperative bacterial communities.

Bacteria live in complex multispecies communities. Intimately interacting bacterial cells are ubiquitous on biological and mineral surfaces in all habitats. Molecular and cellular biologists have unraveled some key mechanisms that modulate bacterial interactions, but the ecology and evolution of these associations remain poorly understood. One debate has focused on the relative importance of cooperation among cells in bacterial communities. Some researchers suggest that communication and cooperation, both within and among bacterial species, have produced emergent properties that give such groups a selective advantage. Evolutionary biologists have countered that the appearance of group-level traits should be viewed with caution, as natural selection almost invariably favors selfishness. A recent theory by Morris, Lenski, and Zinser, called the Black Queen Hypothesis, gives a new perspective on this debate (J. J. Morris, R. E. Lenski, and E. R. Zinser, mBio 3(2):e00036-12, 2012). These authors present a model that reshapes a decades-old idea: cooperation among species can be automatic and based upon purely selfish traits. Moreover, this hypothesis stands in contrast to the Red Queen Hypothesis, which states that species are in constant evolutionary conflict. Two assumptions serve as the core of the Black Queen model. First, bacterial functions are often leaky, such that cells unavoidably produce resources that benefit others. Second, the receivers of such by-products will tend to delete their own costly pathways for those products, thus building dependency into the interactions. Although not explicitly required in their model, an emergent prediction is that the initiation of such dependency can favor the spread of more obligate coevolved partnerships. This new paradigm suggests that bacteria might often form interdependent cooperative interactions in communities and moreover that bacterial cooperation should leave a clear genomic signature via complementary loss of shared diffusible functions.

Phosphite utilization by the marine picocyanobacterium Prochlorococcus MIT9301.

Primary productivity in the ocean's oligotrophic regions is often limited by phosphorus (P) availability. In low phosphate environments, the prevalence of many genes involved in P acquisition is elevated, suggesting that the ability to effectively access diverse P sources is advantageous for organisms inhabiting these regions. Prochlorococcus, the numerically dominant primary producer in the oligotrophic ocean, encodes high-affinity P transporters, P regulatory proteins and enzymes for organic phosphate utilization, but its ability to use reduced P compounds has not been previously demonstrated. Because Prochlorococcus strain MIT9301 encodes genes similar to phnY and phnZ, which constitute a novel marine bacterial 2-aminoethylphosphonate (2-AEPn) utilization pathway, it has been suggested that this organism might use 2-AEPn as an alternative P source. We show here that although MIT9301 was unable to use 2-AEPn as a sole P source under standard culture conditions, it was able to use phosphite. Phosphite utilization by MIT9301 appears to be mediated by an NAD-dependent phosphite dehydrogenase encoded by ptxD. We show that phosphite utilization genes are present in diverse marine microbes and that their abundance is higher in low-P waters. These results strongly suggest that phosphite represents a previously unrecognized component of the marine P cycle.

Code and context: Prochlorococcus as a model for cross-scale biology.

Prochlorococcus is a simple cyanobacterium that is abundant throughout large regions of the oceans, and has become a useful model for studying the nature and regulation of biological diversity across all scales of complexity. Recent work has revealed that environmental factors such as light, nutrients and predation influence diversity in different ways, changing our image of the structure and dynamics of the global Prochlorococcus population. Advances in metagenomics, transcription profiling and global ecosystem modeling promise to deliver an even greater understanding of this system and further demonstrate the power of cross-scale systems biology.