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 ...
Phytoplankton form the foundation of the marine food web and regulate key biogeochemical processes. These organisms face multiple environmental changes 1 , including the decline in ocean pH (ocean acidification) caused by rising atmospheric p CO 2 (ref. 2). A meta-analysis of published experimental data assessing growth rates of di erent phytoplankton taxa under both ambient and elevated p CO 2 conditions revealed a significant range of responses. This e ect of ocean acidification was incorporated into a global marine ecosystem model to explore how marine phytoplankton communities might be impacted over the course of a hypothetical twenty-first century. Results emphasized that the di ering responses to elevated p CO 2 caused su cient changes in competitive fitness between phytoplankton types to significantly alter community structure. At the level of ecological function of the phytoplankton community, acidification had a greater impact than warming or reduced nutrient supply. The model suggested that longer timescales of competition-and transport-mediated adjustments are essential for predicting changes to phytoplankton community structure.The world's oceans have absorbed about 30% of anthropogenic carbon emissions, causing a significant decrease in surface ocean pH (ref. 2). Concerns over the impacts of ocean acidification (OA) on marine life have led to a number of laboratory and field experiments examining the response of marine biota to acidification.OA is not the only driver that is affecting marine ecosystems 1,3 . The oceans are warming, and nutrient and light environments are changing. Numerical models (for example, refs 4-6) have explored how these other drivers impact primary productivity, although less emphasis has been placed on changes in community structure. Phytoplankton types are not physiologically interchangeable, and the specific taxa in a community can impact the cycling of elements and the flow of nutrients and energy through the marine food web. In this study we employed a meta-analysis of OA experiments as input for a numerical model to explore how OA, relative to other drivers, may change phytoplankton community composition.We compiled data from 49 papers (Methods and Supplementary Table 1) in which direct comparisons were made between the growth rates of marine phytoplankton cultures exposed to ambient p CO 2 (∼380 µatm) versus elevated p CO 2 within the range predicted by 2100 (refs 2,7; ∼700-1,000 µatm). The tested organisms were 0.0 0.5 1.0 1.5 * * * * * * GRR C o c c o l i t h o p h o r e D i a t o m O t h e r l a r g e D i a z o t r o p h S y n e c h o c o c c u s P r o c h l o r o c o c c u s 2.0 2.5 Figure 1 | Meta-analysis of GRR of phytoplankton in p CO2 manipulation experiments. Circles represent observations comparing laboratory cultures at high and ambient p CO2 ; triangles indicate long-term experiments; squares represent data from mixed community field incubations. Grey boxes span the 25th-75th percentiles; central lines indicate median values; whiskers extend from the 10th ...
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