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

Autor(es)

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

Afiliação do(s) autor(es)

^[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

• Tipo de documento: Artigo Científico
• Fonte: MICROBIOLOGY SPECTRUM; v. 9, n. 1 SEP 2021.
• Citações Web of Science: 0

Resumo

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)

• Processo FAPESP: 19/08514-0 - Complexos multienzimáticos bacterianos que regulam a homeostase celular em resposta a estresses ambientais
• Beneficiário: Marilis Do Valle Marques
• Modalidade de apoio: Auxílio à Pesquisa - Regular
• Processo FAPESP: 18/17309-8 - Estudo do papel da RNA helicase RhlB da família DEAD-box na estabilidade dos RNAs e na expressão gênica em Caulobacter crescentus
• Beneficiário: Hugo Libonati de Araújo
• Modalidade de apoio: Bolsas no Brasil - Doutorado
• Processo FAPESP: 19/13440-5 - Detecção de transposases codificadas por Sequências de Inserção usando dados de proteômica
• Beneficiário: Alan Péricles Rodrigues Lorenzetti
• Modalidade de apoio: Bolsas no Exterior - Estágio de Pesquisa - Doutorado
• Processo FAPESP: 14/13552-4 - Estudo da RNA helicase da família DEAD-box codificada pelo gene CC0835 em Caulobacter crescentus
• Beneficiário: Alexandre Magno Vicente
• Modalidade de apoio: Bolsas no Brasil - Mestrado
• Processo FAPESP: 17/03052-2 - RNAs não codificantes derivados de sequências de inserção na arqueia halófila Halobacterium salinarum NRC-1
• Beneficiário: Alan Péricles Rodrigues Lorenzetti
• Modalidade de apoio: Bolsas no Brasil - Doutorado