Effects of the Cryptochrome CryB from Rhodobacter sphaeroides on Global Gene Expression in the Dark or Blue Light or in the Presence of Singlet Oxygen

Frühwirth, Sebastian; Teich, Kristin; Klug, Gabriele

doi:10.1371/journal.pone.0033791

Cited by 18 publications

(16 citation statements)

References 58 publications

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“…In contrast, the smaller cluster 3 comprises mRNAs which had a peak expression at 7 min. Functional groups were formed according to published data on the R. sphaeroides singlet oxygen stress response [27]–[31], combined with KEGG database searches (http://www.genome.jp/kegg/). Cluster 1 contains several genes with a function in stress defense or iron metabolism, like phrA , gloB , or bacterioferritin encoding bfr (Figure 2B).…”

Section: Resultsmentioning

confidence: 99%

Integrative “Omics”-Approach Discovers Dynamic and Regulatory Features of Bacterial Stress Responses

et al. 2013

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Bacteria constantly face stress conditions and therefore mount specific responses to ensure adaptation and survival. Stress responses were believed to be predominantly regulated at the transcriptional level. In the phototrophic bacterium Rhodobacter sphaeroides the response to singlet oxygen is initiated by alternative sigma factors. Further adaptive mechanisms include post-transcriptional and post-translational events, which have to be considered to gain a deeper understanding of how sophisticated regulation networks operate. To address this issue, we integrated three layers of regulation: (1) total mRNA levels at different time-points revealed dynamics of the transcriptome, (2) mRNAs in polysome fractions reported on translational regulation (translatome), and (3) SILAC-based mass spectrometry was used to quantify protein abundances (proteome). The singlet oxygen stress response exhibited highly dynamic features regarding short-term effects and late adaptation, which could in part be assigned to the sigma factors RpoE and RpoH2 generating distinct expression kinetics of corresponding regulons. The occurrence of polar expression patterns of genes within stress-inducible operons pointed to an alternative of dynamic fine-tuning upon stress. In addition to transcriptional activation, we observed significant induction of genes at the post-transcriptional level (translatome), which identified new putative regulators and assigned genes of quorum sensing to the singlet oxygen stress response. Intriguingly, the SILAC approach explored the stress-dependent decline of photosynthetic proteins, but also identified 19 new open reading frames, which were partly validated by RNA-seq. We propose that comparative approaches as presented here will help to create multi-layered expression maps on the system level (“expressome”). Finally, intense mass spectrometry combined with RNA-seq might be the future tool of choice to re-annotate genomes in various organisms and will help to understand how they adapt to alternating conditions.

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Section: Resultsmentioning

confidence: 99%

Integrative “Omics”-Approach Discovers Dynamic and Regulatory Features of Bacterial Stress Responses

et al. 2013

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“…Homologs of the protein that we predict mediates this response to light, CryB, are widespread in freshwater Actinobacteria, suggesting that this light response may also be common in surface waters. CryB has been well characterized in Rhodobacter sphaeroides, absorbs blue (ϳ420 nm) light under anoxic conditions, and interacts with AppA to modulate expression of the photosystem (50,51). In contrast, the orthologous protein in Agrobacterium tumefaciens, named PhrB, absorbs light at 375 and 415 nm and has DNA photolyase activity (52).…”

Section: Discussionmentioning

confidence: 99%

Light Modulates the Physiology of NonphototrophicActinobacteria

et al. 2019

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Light is a source of energy and an environmental cue that is available in excess in most surface environments. In prokaryotic systems, conversion of light to energy by photoautotrophs and photoheterotrophs is well understood, but the conversion of light to information and the cellular response to that information have been characterized in only a few species. Our goal was to explore the response of freshwaterActinobacteria, which are ubiquitous in illuminated aquatic environments, to light. We found thatActinobacteriawithout functional photosystems grow faster in the light, likely because sugar transport and metabolism are upregulated in the light. Based on the action spectrum of the growth effect and comparisons of the genomes of threeActinobacteriawith this growth rate phenotype, we propose that the photosensor in these strains is a putative CryB-type cryptochrome. The ability to sense light and upregulate carbohydrate transport during the day could allow these cells to coordinate their time of maximum organic carbon uptake with the time of maximum organic carbon release by primary producers.IMPORTANCESunlight provides information about both place and time. In sunlit aquatic environments, primary producers release organic carbon and nitrogen along with other growth factors during the day. The ability ofActinobacteriato coordinate organic carbon uptake and utilization with production of photosynthate enables them to grow more efficiently in the daytime, and it potentially gives them a competitive advantage over heterotrophs that constitutively produce carbohydrate transporters, which is energetically costly, or produce transporters only after detection of the substrate(s), which delays their response. Understanding how light cues the transport of organic carbon and its conversion to biomass is key to understanding biochemical mechanisms within the carbon cycle, the fluxes through it, and the variety of mechanisms by which light enhances growth.

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“…Very few cryptochromes from bacteria have been characterized, and most of them also show photolyase activity. In addition to the Syn-CRY, CryB of R. sphaeroides was first described as a cryptochrome that affects light-dependent and singlet oxygen-dependent gene expression (106). Also, V. cholerae cryptochrome, VcCry1, has been described as a DASH cryptochome (326).…”

Section: B Non-pas Domain Photosensorsmentioning

confidence: 99%

Redox-Based Transcriptional Regulation in Prokaryotes: Revisiting Model Mechanisms

Sevilla

Bes

González

et al. 2019

Antioxidants & Redox Signaling

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Redox-responsive transcriptional regulation is an intricate process as identical signals may be sensed and transduced by different transcription factors, which often interplay with other DNA-binding proteins with or without regulatory activity. Although there is much information about some key regulators, many others remain to be fully characterized due to the instability of their clusters under oxygen. Understanding the mechanisms and the regulatory networks operated by these regulators is essential for the development of future applications in biotechnology and medicine. Antioxid. Redox Signal. 00, 000-000.

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Effects of the Cryptochrome CryB from Rhodobacter sphaeroides on Global Gene Expression in the Dark or Blue Light or in the Presence of Singlet Oxygen

Cited by 18 publications

References 58 publications

Integrative “Omics”-Approach Discovers Dynamic and Regulatory Features of Bacterial Stress Responses

Integrative “Omics”-Approach Discovers Dynamic and Regulatory Features of Bacterial Stress Responses

Light Modulates the Physiology of NonphototrophicActinobacteria

Redox-Based Transcriptional Regulation in Prokaryotes: Revisiting Model Mechanisms

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