Transcriptomic responses of the marine cyanobacterium <i>Prochlorococcus</i> to viral lysis products

Fang, Xiaoting; Liu, Yaxin; Zhao, Yongkun; Chen, Yue; Liu, Riyue; Qin, Qi‐Long; Li, Gang; Zhang, Yuzhong; Chan, Wan; Hess, Wolfgang R.; Zeng, Qinglu

doi:10.1111/1462-2920.14513

Cited by 14 publications

(8 citation statements)

References 84 publications

(120 reference statements)

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“…It might potentially be a response to a reduction in shelf-shading, (Felcmanová et al 2017), but such a phenomenon has not, to the best of our knowledge, been described previously. A decrease in respiration rates in relation to growth rate as the cells enter chlorosis (Fang et al 2019) is perhaps a more plausible hypothesis. The current model cannot distinguish between these two possibilities without further experimental constraints, nor can it distinguish between the release of organic C through exudation from living cells or from dead cells through lysis.…”

Section: The Accumulation Of Extracellular Carbon and Its Potential Mechanismmentioning

confidence: 99%

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Roth‐Rosenberg

Aharonovich

Omta

et al. 2021

Limnology & Oceanography

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Every living cell is composed of macromolecules such as proteins, DNA, RNA, and pigments. The ratio between these macromolecular pools depends on the allocation of resources within the organism to different physiological requirements, and in turn affects biogeochemical cycles of elements such as carbon, nitrogen, and phosphorus. Here, we present detailed measurements of the macromolecular composition of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, as it grows and declines due to nitrogen starvation in laboratory batch cultures. As cells reached stationary stage and declined, protein per cell decreased by $ 30% whereas RNA per cell and pigments per cell decreased by $ 75%. The decline stage was associated with the appearance of chlorotic cells, which had higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-chlorophyll-like pigments emerged, which were not observed during exponential growth. These divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern Mediterranean. Over 90% of the carbon fixed by Prochlorococcus MIT9312 (but not of a different strain, NATL2A) was released into the growth media under these laboratory conditions. Variations in RNA/protein indicate that, broadly defined, the macromolecular composition of Prochlorococcus MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, possibly due to the significant investment in photosynthetic machinery of phototrophs.

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Section: The Accumulation Of Extracellular Carbon and Its Potential Mechanismmentioning

confidence: 99%

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Roth‐Rosenberg

Aharonovich

Omta

et al. 2021

Limnology & Oceanography

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“…Extracellular phage genomic DNA was quantified using quantitative PCR (qPCR), which provides ~1:1 ratio relative to intact phage numbers for both MPP-B and MPP-C phages (Supplementary Table 3). All qPCR assays were run in triplicate following our previous protocol [82]…”

Section: Infection Kinetics Of Cyanopodovirusesmentioning

confidence: 99%

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

et al. 2022

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Cyanopodoviruses affect the mortality and population dynamics of the unicellular picocyanobacteria Prochlorococcus and Synechococcus, the dominant primary producers in the oceans. Known cyanopodoviruses all contain the DNA polymerase gene (DNA pol) that is important for phage DNA replication and widely used in field quantification and diversity studies. However, we isolated 18 cyanopodoviruses without identifiable DNA pol. They form a new MPP-C clade that was separated from the existing MPP-A, MPP-B, and P-RSP2 clades. The MPP-C phages have the smallest genomes (37.3–37.9 kb) among sequenced cyanophages, and show longer latent periods than the MPP-B phages. Metagenomic reads of both clades are highly abundant in surface waters, but the MPP-C phages show higher relative abundance in surface waters than in deeper waters, while MPP-B phages have higher relative abundance in deeper waters. Our study reveals that cyanophages with distinct genomic contents and infection kinetics can exhibit different depth profiles in the oceans.

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“…These bulk regeneration rates are in the same range as our strainspecific rates presented here. However, even before lysis, viral infection induces shifts in cellular metabolism, such as upregulation of nutrient-specific host genes (Thompson et al, 2011;Zeng and Chisholm, 2012;Puxty et al, 2016;Monier et al, 2017;Fang et al, 2019;Howard-Varona et al, 2020). The ability of phage to manipulate host metabolism has significant implications for nutrient cycles (Zimmerman et al, 2020).…”

Section: Sustained Hydrolysis Of Dop Following Lysismentioning

confidence: 99%

Phosphorus Release and Regeneration Following Laboratory Lysis of Bacterial Cells

2021

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The availability of phosphorus limits primary production in large regions of the oceans, and marine microbes use a variety of strategies to overcome this limitation. One strategy is the production of alkaline phosphatase (APase), which allows hydrolysis of larger dissolved organic phosphorus (DOP) compounds in the periplasm or at the cell surface for transport of orthophosphate into the cell. Cell lysis, driven by grazing and viral infection, releases phosphorus-containing cell components, along with active enzymes that could persist after lysis. The importance of this continued enzymatic activity for orthophosphate regeneration is unknown. We used three model bacteria – Escherichia coli K-12 MG1655, Synechococcus sp. WH7803, and Prochlorococcus sp. MED4 – to assess the impact of continued APase activity after cell lysis, via lysozyme treatment, on orthophosphate regeneration. Direct release of orthophosphate scaled with cell size and was reduced under phosphate-starved conditions where APase activity continued for days after lysis. All lysate incubations showed post-lysis orthophosphate generation suggesting phosphatases other than APase maintain activity. Rates of DOP hydrolysis and orthophosphate remineralization varied post-lysis among strains. Escherichia coli K-12 MG1655 rates of remineralization were 0.6 and 1.2 amol cell–1hr–1 under deplete and replete conditions; Synechococcus WH7803 lysates ranged from 0.04 up to 0.3 amol cell–1hr–1 during phosphorus deplete and replete conditions, respectively, while in Prochlorococcus MED4 lysates, rates were stable at 0.001 amol cell–1hr–1 in both conditions. The range of rates of hydrolysis and regeneration underscores the taxonomic and biochemical variability in the process of nutrient regeneration and further highlights the complexity of quantitatively resolving the major fluxes within the microbial loop.

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Transcriptomic responses of the marine cyanobacterium Prochlorococcus to viral lysis products

Cited by 14 publications

References 84 publications

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

Phosphorus Release and Regeneration Following Laboratory Lysis of Bacterial Cells

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