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Prochlorococcus, the smallest and most abundant phytoplankter in the ocean, is highly sensitive to hydrogen peroxide (HOOH), and co-occurring heterotrophs such as Alteromonas facilitate the growth of Prochlorococcus by scavenging HOOH. Temperature is also a major influence on Prochlorococcus abundance and distribution in the ocean, and studies in other photosynthetic organisms have shown that HOOH and temperature extremes can act together as synergistic stressors. To address potential synergistic effects of temperature and HOOH on Prochlorococcus growth, high- and low-temperature-adapted representative strains were cultured at ecologically relevant concentrations under a range of HOOH concentrations and temperatures. Higher concentrations of HOOH severely diminished the permissive temperature range for growth of both Prochlorococcus strains. At the permissive temperatures, the growth rates of both Prochlorococcus strains decreased as a function of HOOH, and cold temperature increased susceptibility of photosystem II to HOOH-mediated damage. Serving as a proxy for the natural community, co-cultured heterotrophic bacteria increased the Prochlorococcus growth rate under these temperatures, and expanded the permissive range of temperature for growth. These studies indicate that in the ocean, the cross-protective function of the microbial community may confer a fitness increase for Prochlorococcus at its temperature extremes, especially near the ocean surface where oxidative stress is highest. This interaction may play a substantial role in defining the realized thermal niche and habitat range of Prochlorococcus with respect to latitude., (© 2018. International Society for Microbial Ecology.)

Prochlorococcus is a globally important marine cyanobacterium that lacks the gene catalase and relies on 'helper' bacteria such as Alteromonas to remove reactive oxygen species. Increasing atmospheric CO 2 decreases the need for carbon concentrating mechanisms and photorespiration in phytoplankton, potentially altering their metabolism and microbial interactions even when carbon is not limiting growth. Here, Prochlorococcus (VOL4, MIT9312) was co-cultured with Alteromonas (strain EZ55) under ambient (400 p.p.m.) and elevated CO 2 (800 p.p.m.). Under elevated CO 2 , Prochlorococcus had a significantly longer lag phase and greater apparent die-offs after transfers suggesting an increase in oxidative stress. Whole-transcriptome analysis of Prochlorococcus revealed decreased expression of the carbon fixation operon, including carboxysome subunits, corresponding with significantly fewer carboxysome structures observed by electron microscopy. Prochlorococcus co-culture responsive gene 1 had significantly increased expression in elevated CO 2 , potentially indicating a shift in the microbial interaction. Transcriptome analysis of Alteromonas in co-culture with Prochlorococcus revealed decreased expression of the catalase gene, known to be critical in relieving oxidative stress in Prochlorococcus by removing hydrogen peroxide. The decrease in catalase gene expression was corroborated by a significant ~6-fold decrease in removal rates of hydrogen peroxide from co-cultures. These data suggest Prochlorococcus may be more vulnerable to oxidative stress under elevated CO 2 in part from a decrease in ecosystem services provided by heterotrophs like Alteromonas. This work highlights the importance of considering microbial interactions in the context of a changing ocean., (© 2018. International Society for Microbial Ecology.)

The distribution of major clades of Prochlorococcus tracks light, temperature and other environmental variables; yet, the drivers of genomic diversity within these ecotypes and the net effect on biodiversity of the larger community are poorly understood. We examined high light (HL) adapted Prochlorococcus communities across spatial and temporal environmental gradients in the Pacific Ocean to determine the ecological drivers of population structure and diversity across taxonomic ranks. We show that the Prochlorococcus community has the highest diversity at low latitudes, but seasonality driven by temperature, day length and nutrients adds complexity. At finer taxonomic resolution, some 'sub-ecotype' clades have unique, cohesive responses to environmental variables and distinct biogeographies, suggesting that presently defined ecotypes can be further partitioned into ecologically meaningful units. Intriguingly, biogeographies of the HL-I sub-ecotypes are driven by unique combinations of environmental traits, rather than through trait hierarchy, while the HL-II sub-ecotypes appear ecologically similar, thus demonstrating differences among these dominant HL ecotypes. Examining biodiversity across taxonomic ranks reveals high-resolution dynamics of Prochlorococcus evolution and ecology that are masked at phylogenetically coarse resolution. Spatial and seasonal trends of Prochlorococcus communities suggest that the future ocean may be comprised of different populations, with implications for ecosystem structure and function.

To better understand the temporal and spatial dynamics of Prochlorococcus populations, and how these populations co-vary with the physical environment, we followed monthly changes in the abundance of five ecotypes-two high-light adapted and three low-light adapted-over a 5-year period in coordination with the Bermuda Atlantic Time Series (BATS) and Hawaii Ocean Time-series (HOT) programs. Ecotype abundance displayed weak seasonal fluctuations at HOT and strong seasonal fluctuations at BATS. Furthermore, stable 'layered' depth distributions, where different Prochlorococcus ecotypes reached maximum abundance at different depths, were maintained consistently for 5 years at HOT. Layered distributions were also observed at BATS, although winter deep mixing events disrupted these patterns each year and produced large variations in ecotype abundance. Interestingly, the layered ecotype distributions were regularly reestablished each year after deep mixing subsided at BATS. In addition, Prochlorococcus ecotypes each responded differently to the strong seasonal changes in light, temperature and mixing at BATS, resulting in a reproducible annual succession of ecotype blooms. Patterns of ecotype abundance, in combination with physiological assays of cultured isolates, confirmed that the low-light adapted eNATL could be distinguished from other low-light adapted ecotypes based on its ability to withstand temporary exposure to high-intensity light, a characteristic stress of the surface mixed layer. Finally, total Prochlorococcus and Synechococcus dynamics were compared with similar time series data collected a decade earlier at each location. The two data sets were remarkably similar-testimony to the resilience of these complex dynamic systems on decadal time scales.