The RUBISCO to Photosystem II Ratio Limits the Maximum Photosynthetic Rate in Picocyanobacteria

Zorz, Jackie; Allanach, Jessica R.; Murphy, Cole D.; Roodvoets, Mitchell S.; Campbell, Douglas A.; Cockshutt, Amanda M.

doi:10.3390/life5010403

Cited by 35 publications

(28 citation statements)

References 44 publications

(56 reference statements)

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“…We observed that transcripts for numerous PSI subunits, as well as the PSI assembly protein Ycf3, were enriched during co-culture, while only two PSII-related proteins (the cytochrome b 559 subunit PsbF and a PSII assembly protein, Psb27) showed a significant response (Table 2). PSI:PSII ratios have been found to vary during the exponential growth of Prochlorococcus cultures (Zorz et al, 2015), but these changes were identified as significant across three biological replicate axenic and co-cultures. Further, given the similarity in growth rates and flow cytometry parameters among the axenic and cocultured cells (Figure 1a, Supplementary Figure S1), these data suggest that this reshaping of the photosynthetic apparatus was a consequence of co-culture.…”

Section: Resultsmentioning

confidence: 93%

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

2016

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Microbial interactions, whether direct or indirect, profoundly affect the physiology of individual cells and ultimately have the potential to shape the biogeochemistry of the Earth. For example, the growth of Prochlorococcus, the numerically dominant cyanobacterium in the oceans, can be improved by the activity of co-occurring heterotrophs. This effect has been largely attributed to the role of heterotrophs in detoxifying reactive oxygen species that Prochlorococcus, which lacks catalase, cannot. Here, we explore this phenomenon further by examining how the entire transcriptome of Prochlorococcus NATL2A changes in the presence of a naturally co-occurring heterotroph, Alteromonas macleodii MIT1002, with which it was co-cultured for years, separated and then reunited. Significant changes in the Prochlorococcus transcriptome were evident within 6 h of initiating co-culture, with groups of transcripts changing in different temporal waves. Many transcriptional changes persisted throughout the 48 h experiment, suggesting that the presence of the heterotroph affected a stable shift in Prochlorococcus physiology. These initial transcriptome changes largely corresponded to reduced stress conditions for Prochlorococcus, as inferred from the depletion of transcripts encoding DNA repair enzymes and many members of the 'high light inducible' family of stress-response proteins. Later, notable changes were seen in transcripts encoding components of the photosynthetic apparatus (particularly, an increase in PSI subunits and chlorophyll synthesis enzymes), ribosomal proteins and biosynthetic enzymes, suggesting that the introduction of the heterotroph may have induced increased production of reduced carbon compounds for export. Changes in secretion-related proteins and transporters also highlight the potential for metabolic exchange between the two strains.

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Section: Resultsmentioning

confidence: 93%

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

2016

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“…This in turn led to faster electron transport away from PSII (Fig. 5a) (Zorz et al 2015), which might have ameliorated PSII photoinhibition and stimulated the cell growth (Fig. 5b) under LN.…”

Section: Discussionmentioning

confidence: 99%

Interactive effects of nitrogen and light on growth rates and RUBISCO content of small and large centric diatoms

Campbell

2016

Photosynth Res

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Among marine phytoplankton groups, diatoms span the widest range of cell size, with resulting effects upon their nitrogen uptake, photosynthesis and growth responses to light. We grew two strains of marine centric diatoms differing by ~4 orders of magnitude in cell biovolume in high (enriched artificial seawater with ~500 µmol L−1 µmol L−1 NO3 −) and lower-nitrogen (enriched artificial seawater with <10 µmol L−1 NO3 −) media, across a range of growth light levels. Nitrogen and total protein per cell decreased with increasing growth light in both species when grown under the lower-nitrogen media. Cells growing under lower-nitrogen media increased their cellular allocation to RUBISCO and their rate of electron transport away from PSII, for the smaller diatom under low growth light and for the larger diatom across the range of growth lights. The smaller coastal diatom Thalassiosira pseudonana is able to exploit high nitrogen in growth media by up-regulating growth rate, but the same high-nitrogen growth media inhibits growth of the larger diatom species.Electronic supplementary materialThe online version of this article (doi:10.1007/s11120-016-0301-7) contains supplementary material, which is available to authorized users.

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“…At the same time Prochlorococcus is significantly smaller than Synechococcus (6), and cell mass decreases along its phylogeny (59), thus suggesting an increase in the mass-normalized absorption cross-section σPSII . Fewer comparative studies exist for the quantum efficiency of PSII (ΦPSII ) but it appears to be roughly similar along the Prochlorococcus phylogeny (57). The increasing excretion of organic carbon by Prochlorococcus thus appears to reflect a more general trend that increases the total cellular throughput of electrons (Fig.…”

Section: Significancementioning

confidence: 95%

Metabolic evolution and the self-organization of ecosystems

Braakman

Follows

Chisholm

2017

Proc. Natl. Acad. Sci. U.S.A.

143

165

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Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus. To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and selforganization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen. metabolic evolution | Prochlorococcus | microbial oceanography | mutualism | Earth history M etabolism sustains the nonequilibrium chemical order of the biosphere by continually supplying the energy and building blocks of all cells on Earth (1-5). Here we ask: How does cellular metabolic evolution shape the mass and energy flows of ecosystems? The oceanic phytoplankter Prochlorococcus (6), the most abundant photosynthetic cell on Earth (7,8), provides an ideal model system for addressing this question. Prochlorococcus and its deeper-branching sister lineage marine Synechococcus make up the marine picocyanobacteria and have a characteristic biogeography (9). Prochlorococcus "ecotypes" have geographically (10, 11) and seasonally (12) dynamic populations that in warm, stable stratified water columns always return to the same general structure: Recently diverging highlight-adapted (HL) ecotypes are most abundant toward the surface, whereas deeper branching low-light-adapted (LL) ecotypes are most abundant at depth (10-14) (Fig. 1).What selective forces drove this niche partitioning in Prochlorococcus, and what were the consequences for the ocean ecosystem in general? To address these questions, we reconstructed (15, 16) (Fig. 2) the evolution of core metabolism in strains representing the major clades of Prochlorococcus. To interpret the observed patterns, we developed an evolutionary framework that illuminates the driving forces that produc...

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The RUBISCO to Photosystem II Ratio Limits the Maximum Photosynthetic Rate in Picocyanobacteria

Cited by 35 publications

References 44 publications

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

Interactive effects of nitrogen and light on growth rates and RUBISCO content of small and large centric diatoms

Metabolic evolution and the self-organization of ecosystems

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