The role of RNA stability during bacterial stress responses and starvation

Takayama, Kathy; Kjelleberg, Staffan

doi:10.1046/j.1462-2920.2000.00119.x

Cited by 82 publications

(58 citation statements)

References 110 publications

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“…2A and B). Finally, these results fit directly with studies of other organisms (53). Collectively, these results suggest that the stringent, cold shock, and heat shock responses influence molecular components that influence mRNA turnover in S. aureus cells.…”

Section: Resultssupporting

confidence: 82%

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Characterization of the Staphylococcus aureus Heat Shock, Cold Shock, Stringent, and SOS Responses and Their Effects on Log-Phase mRNA Turnover

et al. 2006

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Despite its being a leading cause of nosocomal and community-acquired infections, surprisingly little is known about Staphylococcus aureus stress responses. In the current study, Affymetrix S. aureus GeneChips were used to define transcriptome changes in response to cold shock, heat shock, stringent, and SOS responseinducing conditions. Additionally, the RNA turnover properties of each response were measured. Each stress response induced distinct biological processes, subsets of virulence factors, and antibiotic determinants. The results were validated by real-time PCR and stress-mediated changes in antimicrobial agent susceptibility. Collectively, many S. aureus stress-responsive functions are conserved across bacteria, whereas others are unique to the organism. Sets of small stable RNA molecules with no open reading frames were also components of each response. Induction of the stringent, cold shock, and heat shock responses dramatically stabilized most mRNA species. Correlations between mRNA turnover properties and transcript titers suggest that S. aureus stress response-dependent alterations in transcript abundances can, in part, be attributed to alterations in RNA stability. This phenomenon was not observed within SOS-responsive cells.

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Section: Resultssupporting

confidence: 82%

“…Similarly, Klebsiella pneumoniae nitrogen fixation protein production corresponds to regulated mRNA turnover (10,28,29). Moreover, in Vibrio angustum, the cellular response to nutrient depravation is regulated by altering mRNA stability (53).…”

mentioning

confidence: 99%

Characterization of the Staphylococcus aureus Heat Shock, Cold Shock, Stringent, and SOS Responses and Their Effects on Log-Phase mRNA Turnover

et al. 2006

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“…In particular, the decay times of some transcripts and proteins were estimated to be as high as several weeks (SI Appendix, Table S5). For proteins, these estimates fall within known ranges (47); however, for transcripts, these estimates are much higher than decay times determined experimentally in cells (48). One reason for this discrepancy seems to be the underestimation of the SNTZ depth range by the model, which in turn leads to longer estimates for mRNA decay times needed to explain the detection of these molecules outside of the SNTZ.…”

Section: Mrna and Protein Profilesmentioning

confidence: 55%

Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone

Louca

Hawley

Katsev

et al. 2016

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

120

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Microorganisms are the most abundant lifeform on Earth, mediating global fluxes of matter and energy. Over the past decade, high-throughput molecular techniques generating multiomic sequence information (DNA, mRNA, and protein) have transformed our perception of this microcosmos, conceptually linking microorganisms at the individual, population, and community levels to a wide range of ecosystem functions and services. Here, we develop a biogeochemical model that describes metabolic coupling along the redox gradient in Saanich Inlet-a seasonally anoxic fjord with biogeochemistry analogous to oxygen minimum zones (OMZs). The model reproduces measured biogeochemical process rates as well as DNA, mRNA, and protein concentration profiles across the redox gradient. Simulations make predictions about the role of ubiquitous OMZ microorganisms in mediating carbon, nitrogen, and sulfur cycling. For example, nitrite "leakage" during incomplete sulfide-driven denitrification by SUP05 Gammaproteobacteria is predicted to support inorganic carbon fixation and intense nitrogen loss via anaerobic ammonium oxidation. This coupling creates a metabolic niche for nitrous oxide reduction that completes denitrification by currently unidentified community members. These results quantitatively improve previous conceptual models describing microbial metabolic networks in OMZs. Beyond OMZ-specific predictions, model results indicate that geochemical fluxes are robust indicators of microbial community structure and reciprocally, that gene abundances and geochemical conditions largely determine gene expression patterns. The integration of real observational data, including geochemical profiles and process rate measurements as well as metagenomic, metatranscriptomic and metaproteomic sequence data, into a biogeochemical model, as shown here, enables holistic insight into the microbial metabolic network driving nutrient and energy flow at ecosystem scales.M icrobial communities catalyze Earth's biogeochemical cycles through metabolic pathways that couple fluxes of matter and energy to biological growth (1). These pathways are encoded in evolving genes that, over time, spread across microbial lineages and today shape the conditions for life on Earth. High-throughput sequencing and mass-spectrometry platforms are generating multiomic sequence information (DNA, mRNA, and protein) that is transforming our perception of this microcosmos, but the vast majority of environmental sequencing studies lack a mechanistic link to geochemical processes. At the same time, mathematical models are increasingly used to describe local-and global-scale biogeochemical processes or predict future changes in global elemental cycling and climate (2, 3). Although these models typically incorporate the catalytic properties of cells, they fail to integrate the information flow from DNA to mRNA, proteins, and process rates as described by the central dogma of molecular biology (4). Hence, a mechanistic framework integrating multiomic data with geochemical information has...

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“…Phosphoester lipids have been shown to degrade substantially within 2-4 days, though small percentages remain even after several weeks (White et al, 1979;Harvey et al, 1986). Thus, IPL turnover occurs likely on a scale of days to weeks (that is, similar to DNA), whereas RNA (especially mRNA) will have a much shorter half-life on the order of minutes to hours (Takayama and Kjelleberg, 2000).…”

Section: Discussionmentioning

confidence: 99%

Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone

et al. 2011

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Ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (anammox) bacteria have emerged as significant factors in the marine nitrogen cycle and are responsible for the oxidation of ammonium to nitrite and dinitrogen gas, respectively. Potential for an interaction between these groups exists; however, their distributions are rarely determined in tandem. Here we have examined the vertical distribution of AOA and anammox bacteria through the Arabian Sea oxygen minimum zone (OMZ), one of the most intense and vertically exaggerated OMZs in the global ocean, using a unique combination of intact polar lipid (IPL) and gene-based analyses, at both DNA and RNA levels. To screen for AOA-specific IPLs, we developed a high-performance liquid chromatography/mass spectrometry/mass spectrometry method targeting hexose-phosphohexose (HPH) crenarchaeol, a common IPL of cultivated AOA. HPH-crenarchaeol showed highest abundances in the upper OMZ transition zone at oxygen concentrations of ca. 5 lM, coincident with peaks in both thaumarchaeotal 16S rDNA and amoA gene abundances and gene expression. In contrast, concentrations of anammox-specific IPLs peaked within the core of the OMZ at 600 m, where oxygen reached the lowest concentrations, and coincided with peak anammox 16S rDNA and the hydrazine oxidoreductase (hzo) gene abundances and their expression. Taken together, the data reveal a unique depth distribution of abundant AOA and anammox bacteria and the segregation of their respective niches by 4400 m, suggesting no direct coupling of their metabolisms at the time and site of sampling in the Arabian Sea OMZ.

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The role of RNA stability during bacterial stress responses and starvation

Cited by 82 publications

References 110 publications

Characterization of the Staphylococcus aureus Heat Shock, Cold Shock, Stringent, and SOS Responses and Their Effects on Log-Phase mRNA Turnover

Characterization of the Staphylococcus aureus Heat Shock, Cold Shock, Stringent, and SOS Responses and Their Effects on Log-Phase mRNA Turnover

Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone

Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone

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