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Establishing links between microbial diversity and environmental processes requires resolving the high degree of functional variation among closely related lineages or ecotypes. Here, we implement and validate an improved metagenomic approach that estimates the spatial biogeography and environmental regulation of ecotype-specific replication patterns (R Obs ) across ocean regions. A total of 719 metagenomes were analyzed from meridional Bio-GO-SHIP sections in the Atlantic and Indian Ocean. Accounting for sequencing bias and anchoring replication estimates in genome structure were critical for identifying physiologically relevant biological signals. For example, ecotypes within the dominant marine cyanobacteria Prochlorococcus exhibited distinct diel cycles in R Obs that peaked between 19:00-22:00. Additionally, both Prochlorococcus ecotypes and ecotypes within the highly abundant heterotroph Pelagibacter (SAR11) demonstrated systematic biogeographies in R Obs that differed from spatial patterns in relative abundance. Finally, R Obs was significantly regulated by nutrient stress and temperature, and explained by differences in the genomic potential for nutrient transport, energy production, cell wall structure, and replication. Our results suggest that our new approach to estimating replication is reflective of gross population growth. Moreover, this work reveals that the interaction between adaptation and environmental change drives systematic variability in replication patterns across ocean basins that is ecotype-specific, adding an activity-based dimension to our understanding of microbial niche space., (© 2022. The Author(s).)

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., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

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'.

Variation in ocean C:N:P of particulate organic matter (POM) has led to competing hypotheses for the underlying drivers. Each hypothesis predicts C:N:P equally well due to regional co-variance in environmental conditions and biodiversity. The Indian Ocean offers a unique positive temperature and nutrient supply relationship to test these hypotheses. Here we show how elemental concentrations and ratios vary over daily and regional scales. POM concentrations were lowest in the southern gyre, elevated across the equator, and peaked in the Bay of Bengal. Elemental ratios were highest in the gyre, but approached Redfield proportions northwards. As Prochlorococcus dominated the phytoplankton community, biodiversity changes could not explain the elemental variation. Instead, our data supports the nutrient supply hypothesis. Finally, gyre dissolved iron concentrations suggest extensive iron stress, leading to depressed ratios compared to other gyres. We propose a model whereby differences in iron supply and N 2 -fixation influence C:N:P levels across ocean gyres.

The Cyanobacteria Prochlorococcus and Synechococcus account for a substantial fraction of marine primary production. Here, we present quantitative niche models for these lineages that assess present and future global abundances and distributions. These niche models are the result of neural network, nonparametric, and parametric analyses, and they rely on >35,000 discrete observations from all major ocean regions. The models assess cell abundance based on temperature and photosynthetically active radiation, but the individual responses to these environmental variables differ for each lineage. The models estimate global biogeographic patterns and seasonal variability of cell abundance, with maxima in the warm oligotrophic gyres of the Indian and the western Pacific Oceans and minima at higher latitudes. The annual mean global abundances of Prochlorococcus and Synechococcus are 2.9 ± 0.1 × 10(27) and 7.0 ± 0.3 × 10(26) cells, respectively. Using projections of sea surface temperature as a result of increased concentration of greenhouse gases at the end of the 21st century, our niche models projected increases in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively. The changes are geographically uneven but include an increase in area. Thus, our global niche models suggest that oceanic microbial communities will experience complex changes as a result of projected future climate conditions. Because of the high abundances and contributions to primary production of Prochlorococcus and Synechococcus, these changes may have large impacts on ocean ecosystems and biogeochemical cycles.