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(Reference retrieved automatically from Web of Science through information on FAPESP grant and its corresponding number as mentioned in the publication by the authors.)

Cold Regulation of Genes Encoding Ion Transport Systems in the Oligotrophic Bacterium Caulobacter crescentus

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de Araujo, Hugo L. [1] ; Martins, Bianca P. [1] ; Vicente, Alexandre M. [1, 2] ; Lorenzetti, Alan P. R. [3] ; Koide, Tie [3] ; Marques, V, Marilis
Total Authors: 6
[1] V, Univ Sao Paulo, Inst Ciencias Biomed, Dept Microbiol, Sao Paulo - Brazil
[2] Ludwig Maximilians Univ Munchen, Biozentrum, Munich - Germany
[3] Univ Sao Paulo, Fac Med Ribeirao Preto, Dept Bioquirn & Imunol, Ribeirao Preto - Brazil
Total Affiliations: 3
Document type: Journal article
Source: MICROBIOLOGY SPECTRUM; v. 9, n. 1 SEP 2021.
Web of Science Citations: 0

In this study, we characterize the response of the free-living oligotrophic alphaproteobacterium Caulobacter crescentus to low temperatures by global transcriptomic analysis. Our results showed that 656 genes were upregulated and 619 were downregulated at least 2-fold after a temperature downshift. The identified differentially expressed genes (DEG) belong to several functional categories, notably inorganic ion transport and metabolism, and a subset of these genes had their expression confirmed by reverse transcription quantitative real-time PCR (RT-qPCR). Several genes belonging to the ferric uptake regulator (Fur) regulon were downregulated, indicating that iron homeostasis is relevant for adaptation to cold. Several upregulated genes encode proteins that interact with nucleic acids, particularly RNA: cspA, cspB, and the DEAD box RNA helicases rhlE, dbpA, and rhlB. Moreover, 31 small regulatory RNAs (sRNAs), including the cell cycle-regulated noncoding RNA (ncRNA) CcnA, were upregulated, indicating that posttranscriptional regulation is important for the cold stress response. Interestingly, several genes related to transport were upregulated under cold stress, including three AcrB-like cation/multidrug efflux pumps, the nitrate/nitrite transport system, and the potassium transport genes kdpFABC. Further characterization showed that kdpA is upregulated in a potassium-limited medium and at a low temperature in a SigT-independent way. kdpA mRNA is less stable in rho and rhlE mutant strains, but while the expression is positively regulated by RhlE, it is negatively regulated by Rho. A kdpA-deleted strain was generated, and its viability in response to osmotic, acidic, or cold stresses was determined. The implications of such variation in the gene expression for cold adaptation are discussed. IMPORTANCE Low-temperature stress is an important factor for nucleic acid stability and must be circumvented in order to maintain the basic cell processes, such as transcription and translation. The oligotrophic lifestyle presents further challenges to ensure the proper nutrient uptake and osmotic balance in an environment of slow nutrient flow. Here, we show that in Caulobacter crescentus, the expression of the genes involved in cation transport and homeostasis is altered in response to cold, which could lead to a decrease in iron uptake and an increase in nitrogen and highaffinity potassium transport by the Kdp system. This previously uncharacterized regulation of the Kdp transporter has revealed a new mechanism for adaptation to low temperatures that may be relevant for oligotrophic bacteria. (AU)

Grantee:Marilis Do Valle Marques
Support Opportunities: Regular Research Grants
FAPESP's process: 18/17309-8 - Study of the role of the DEAD-box RNA helicase RhlB in the RNA stability and gene expression in Caulobacter crescentus
Grantee:Hugo Libonati de Araújo
Support Opportunities: Scholarships in Brazil - Doctorate
FAPESP's process: 19/13440-5 - Detection of Insertion Sequence-encoded transposases using proteome data
Grantee:Alan Péricles Rodrigues Lorenzetti
Support Opportunities: Scholarships abroad - Research Internship - Doctorate
FAPESP's process: 14/13552-4 - Study of the DEAD-box RNA helicase encoded by the gene CC0835 in Caulobacter crescentus
Grantee:Alexandre Magno Vicente
Support Opportunities: Scholarships in Brazil - Master
FAPESP's process: 17/03052-2 - Non-coding RNAs derived from insertion sequences in the halophilic archaeon Halobacterium salinarum NRC-1
Grantee:Alan Péricles Rodrigues Lorenzetti
Support Opportunities: Scholarships in Brazil - Doctorate