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The CO2 content of Earth's atmosphere is rapidly increasing due to human consumption of fossil fuels. Models based on short-term culture experiments predict that major changes will occur in marine phytoplankton communities in the future ocean, but these models rarely consider how the evolutionary potential of phytoplankton or interactions within marine microbial communities may influence these changes. Here we experimentally evolved representatives of four phytoplankton functional types (silicifiers, calcifiers, coastal cyanobacteria, and oligotrophic cyanobacteria) in co-culture with a heterotrophic bacterium, Alteromonas, under either present-day or predicted future pCO2 conditions. The data and analysis code in this dataset show that the genomes of all four phytoplankton as well as Alteromonas evolved over the course of the experiment. Mutations in oxidative stress related genes (PTOX and thioredoxin reductase) were ubiquitous in evolved cultures of Prochlorococcus, suggesting adaptation in response to the well-studied deficiencies of this genus in terms of stress resistance in culture. With the exception of Prochlorococcus, most phytoplankton genomes appeared to experience mostly purifying selection, but Alteromonas genomes showed strong evidence of directional selection, particularly in co-culture with eukaryotic phytoplankton. Metabolic pathways were under intense selection for Alteromonas, and in particular adaptation to co-culture with eukaryotes appeared to select for a shift from growth on organic acids using an abbreviated TCA cycle to growth on more complex substrates using the complete TCA cycle. This work provides new insights on how phytoplankton will respond to anthropogenic change and on the evolutionary mechanisms governing the structure and function of marine microbial communities.
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Emergence of metabolic coupling to the heterotroph Alteromonas promotes dark survival in Prochlorococcus
Abstract Prochlorococcus is found throughout the euphotic zone in the oligotrophic open ocean. Deep mixing and sinking while attached to particles can, however, transport Prochlorococcus cells below this sunlit zone, depriving them of light for extended periods of time. Previous work has shown that Prochlorococcus by itself cannot survive extended periods of darkness. However, when co-cultured with a heterotrophic microbe and subjected to repeated periods of extended darkness, Prochlorococcus cells develop an epigenetically inherited dark-tolerant phenotype that can survive longer periods of darkness. Here we examine the metabolic and physiological changes underlying this adaptation using co-cultures of dark-tolerant and parental strains of Prochlorococcus, each grown with the heterotroph Alteromonas under diel light:dark conditions. The relative abundance of Alteromonas was higher in dark-tolerant than parental co-cultures, while dark-tolerant Prochlorococcus cells were larger, contained less chlorophyll, and were less synchronized to the light:dark cycle. Meta-transcriptome analysis revealed that dark-tolerant co-cultures undergo a joint change, in which Prochlorococcus undergoes a relative shift from photosynthesis to respiration, while Alteromonas shifts toward using more organic acids instead of sugars. Furthermore, the transcriptome data suggested enhanced biosynthesis of amino acids and purines in dark-tolerant Prochlorococcus and enhanced degradation of these compounds in Alteromonas. Collectively, our results demonstrate that dark adaptation involves a strengthening of the metabolic coupling between Prochlorococcus and Alteromonas, presumably mediated by an enhanced, and compositionally modified, carbon exchange between the two species.
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- PAR ID:
- 10559487
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- ISME Communications
- Volume:
- 4
- Issue:
- 1
- ISSN:
- 2730-6151
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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