The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species.

Axenic (pure) cultures of marine unicellular cyanobacteria of the Prochlorococcus genus grow efficiently only if the inoculation concentration is large; colonies form on semisolid medium at low efficiencies. In this work, we describe a novel method for growing Prochlorococcus colonies on semisolid agar that improves the level of recovery to approximately 100%. Prochlorococcus grows robustly at low cell concentrations, in liquid or on solid medium, when cocultured with marine heterotrophic bacteria. Once the Prochlorococcus cell concentration surpasses a critical threshold, the "helper" heterotrophs can be eliminated with antibiotics to produce axenic cultures. Our preliminary evidence suggests that one mechanism by which the heterotrophs help Prochlorococcus is the reduction of oxidative stress.Members of the genus Prochlorococcus are the most abundant marine photosynthetic organisms and, as such, are major contributors to photosynthesis in the ocean (20). Over 30 strains of Prochlorococcus have been brought into culture, isolated from many locations within the band from 40°N to 40°S, including the North Atlantic, the North and South Pacific Oceans, the Mediterranean Sea, and the Arabian Sea (20). Despite this success, very few pure cultures of Prochlorococcus (e.g., those of strains PCC 9511 and MIT 9313 [18,22]) have been obtained. The vast majority of cultures contain heterotrophic microbes as contaminants; these heterotrophs were cocultured from the marine environment during the isolation procedure, which has relied thus far exclusively on liquid cultivation. While plating for contiguous lawns of Prochlorococcus has proven to be productive (15), attempts at colony formation (by pour plating or surface streak plating) have thus far met with significantly less success. Recovery efficiencies of the pour plating technique of 0.1 to 10% have been reported previously for some strains (15,24), but this technique has yet to produce pure cultures (15). The inability to readily obtain clonal, pure cultures of Prochlorococcus has severely limited progress in the genetic and physiological analysis of this ecologically important lineage.The "helper" phenotype of heterotrophic bacteria. Standard dilution streaking of contaminated Prochlorococcus cultures onto semisolid medium failed to produce axenic colonies. Colonies formed only within a visible mass of the contaminant heterotrophic bacteria; such masses appeared typically at the sites of the earliest, heaviest dilution streaks (data not shown). One interpretation of these results was that Prochlorococcus was able to grow only in the presence of the contaminating bacteria, perhaps because the bacteria provide a growth factor and/or remove an inhibitory factor. Coculturing with heterotrophic bacteria is required for the growth of some bacterial isolates (9) and is known to improve the growth of dinoflagellates (2, 7), suggesting that a similar interaction may help Prochlorococcus. To test this hypothesis, a heterotrophic contaminant (designated EZ55) of a culture of the ...

Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean.cyanobacteria | cell division | mortality | flow cytometry | SeaFlow P otential interdependencies between species diversity and ecosystem stability have gained increased focus due to global changes in species distributions and abundances (1). Strong predator-prey interactions are predicted to enhance the number of coexisting species and limit fluctuations in abundances (2, 3), whereas competition for limited resources is predicted to reduce biodiversity, in some instances, to the point of ecological instability (3, 4). Mechanisms underlying ecosystem stability remain challenging to characterize on relevant temporal and spatial scales, in part because few empirical data are available to test these theories.Our focus is on the microbial communities within surface waters of the vast oligotrophic gyre of the north Pacific Subtropical Ocean. Here, competition for low concentrations of essential nutrients is hypothesized to result in relatively few abundant microbial species, typified by their extremely small cell sizes and streamlined genomes (5). The cyanobacterium Prochlorococcus numerically dominates the photosynthetic community in these regions, with a relatively constant cell abundance close to half a billion cells per liter despite a population doubling time of approximately one day (6). Such constant cell numbers are predicted when both...

Foraging theory predicts the evolution of feeding behaviors that increase consumer fitness. Sponges were among the earliest metazoans on earth and developed a unique filter‐feeding mechanism that does not rely on a nervous system. Once thought indiscriminate, sponges are now known to selectively consume picoplankton, but it is unclear whether this confers any benefit. Additionally, sponges consume dissolved organic carbon (DOC) and detritus, but relative preferences for these resources are unknown. We quantified suspension feeding by the giant barrel sponge Xestospongia muta on Conch Reef, Florida, to examine relationships between diet choice, food resource availability, and foraging efficiency. Sponges consistently preferred cyanobacteria over other picoplankton, which were preferred over detritus and DOC; nevertheless, the sponge diet was mostly DOC (∼70%) and detritus (∼20%). Consistent with foraging theory, less‐preferred foods were discriminated against when relatively scarce, but were increasingly accepted as they became relatively more abundant. Food uptake was limited, likely by post‐capture constraints, yet selective foraging enabled sponges to increase nutritional gains.