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.

Linking ‘omics measurements with biogeochemical cycles is a widespread challenge in microbial community ecology. Here, we propose applying genomic adaptation as ‘biosensors’ for microbial investments to overcome nutrient stress. We then integrate this genomic information with a trait-based model to predict regional shifts in the elemental composition of marine plankton communities. We evaluated this approach using metagenomic and particulate organic matter samples from the Atlantic, Indian and Pacific Oceans. We find that our genome-based trait model significantly improves our prediction of particulate C : P (carbon : phosphorus) across ocean regions. Furthermore, we detect previously unrecognized ocean areas of iron, nitrogen and phosphorus stress. In many ecosystems, it can be very challenging to quantify microbial stress. Thus, a carefully calibrated genomic approach could become a widespread tool for understanding microbial responses to environmental changes and the biogeochemical outcomes. This article is part of the theme issue ‘Conceptual challenges in microbial community ecology’.

In this study, we combined “reciprocal transplant experiments,” cell‐sorting, and metagenomics to understand how phytoplankton adapt to differences in phosphate availability and the implications for nutrient uptake rates. Reciprocal transplant experiments were conducted on six stations ranging from cold, nutrient‐rich water in the Labrador Sea to warm, extremely P‐deplete water in the Sargasso Sea. In most cases, the direct impact of environmental conditions and likely P availability was the strongest control on phosphate uptake. However, especially the transplant experiments between the northern and southern stations revealed that there are situations where changes in community composition and functional genes have an important effect on uptake rates. Phytoplankton lineages responded uniquely to changing environmental conditions. The picoeukaryotic phytoplankton P uptake response was strongly regulated by the phosphate concentration, whereas the effect of community composition was larger for Prochlorococcus and Synechococcus. In support, we found a tight negative relationship between ambient phosphate concentration and the frequency of P acquisition genes in both Prochlorococcus and Synechococcus, and such differences in genome content could be linked to lineage‐specific shifts in uptake rates. Linking genes with ocean biogeochemistry is a major scientific and technical challenge and most studies rely on correlations between genotypes and environmental conditions. However, our study demonstrates how reciprocal transplant experiments are a possible tool for understanding the relative role of environmental condition vs. plankton diversity in regulating important open ocean ecosystem processes.

Detailed descriptions of microbial communities have lagged far behind physical and chemical measurements in the marine environment. Here, we present 971 globally distributed surface ocean metagenomes collected at high spatio-temporal resolution. Our low-cost metagenomic sequencing protocol produced 3.65 terabases of data, where the median number of base pairs per sample was 3.41 billion. The median distance between sampling stations was 26 km. The metagenomic libraries described here were collected as a part of a biological initiative for the Global Ocean Ship-based Hydrographic Investigations Program, or “Bio-GO-SHIP.” One of the primary aims of GO-SHIP is to produce high spatial and vertical resolution measurements of key state variables to directly quantify climate change impacts on ocean environments. By similarly collecting marine metagenomes at high spatiotemporal resolution, we expect that this dataset will help answer questions about the link between microbial communities and biogeochemical fluxes in a changing ocean.

Detailed descriptions of microbial communities have lagged far behind physical and chemical measurements in the marine environment. Here, we present 720 globally distributed surface ocean metagenomes collected at high spatio-temporal resolution. Our low-cost metagenomic sequencing protocol produced 2.75 terabases of data, where the median number of base pairs per sample was 3.48 billion. The median distance between sampling stations was 26 km. The metagenomic libraries described here were collected as a part of a biological initiative for the Global Ocean Ship-based Hydrographic Investigations Program, or “Bio-GO-SHIP.” One of the primary aims of GO-SHIP is to produce high spatial and vertical resolution measurements of key state variables to directly quantify climate change impacts on ocean environments. By similarly collecting marine metagenomes at high spatiotemporal resolution, we expect that this dataset will help answer questions about the link between microbial communities and biogeochemical fluxes in a changing ocean.

Prochlorococcus is the most numerically abundant photosynthetic organism in the surface ocean. The Prochlorococcus high-light and warm-water adapted ecotype (HLII) is comprised of extensive microdiversity, but specific functional differences between microdiverse sub-clades remain elusive. Here we characterized both functional and phylogenetic diversity within the HLII ecotype using Bio-GO-SHIP metagenomes. We found widespread variation in gene frequency connected to local environmental conditions. Metagenome-assembled marker genes and genomes revealed a globally distributed novel HLII haplotype defined by adaptation to chronically low P conditions (HLII-P). Environmental correlation analysis revealed different factors were driving gene abundances verses phylogenetic differences. An analysis of cultured HLII genomes and metagenome-assembled genomes revealed a subclade within HLII, which corresponded to the novel HLII-P haplotype. This work represents the first global assessment of the HLII ecotype’s phylogeography and corresponding functional differences. These findings together expand our understanding of how microdiversity structures functional differences and reveals the importance of nutrients as drivers of microdiversity in Prochlorococcus.

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Prochlorococcusis the most numerically abundant photosynthetic organism in the surface ocean. TheProchlorococcushigh-light and warm-water adapted ecotype (HLII) is comprised of extensive microdiversity, but specific functional differences between microdiverse sub-clades remain elusive. Here we characterized both functional and phylogenetic diversity within the HLII ecotype using Bio-GO-SHIP metagenomes. We found widespread variation in gene frequency connected to local environmental conditions. Metagenomically assembled marker genes and genomes revealed a globally distributed novel HLII haplotype defined by adaptation to chronically low P conditions (HLII-P). Environmental correlation analysis revealed different factors were driving gene abundances verses phylogenetic differences. An analysis of cultured HLII genomes and metagenomically assembled genomes revealed a subclade within HLII, which corresponded to the novel HLII-P haplotype. This work represents the first global assessment of the HLII ecotype's phylogeography and corresponding functional differences. These findings together expand our understanding of how microdiversity structures functional differences and reveals the importance of nutrients as drivers of microdiversity inProchlorococcus.