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Proteomic and Transcriptomic Analyses of “Candidatus Pelagibacter ubique” Describe the First P[subscript II]-Independent Response to Nitrogen Limitation in a Free-Living Alphaproteobacterium

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  • Nitrogen is one of the major nutrients limiting microbial productivity in the ocean, and as a result, most marine microorganisms have evolved systems for responding to nitrogen stress. The highly abundant alphaproteobacterium “Candidatus Pelagibacter ubique,” a cultured member of the order Pelagibacterales (SAR11), lacks the canonical GlnB, GlnD, GlnK, and NtrB/NtrC genes for regulating nitrogen assimilation, raising questions about how these organisms respond to nitrogen limitation. A survey of 266 Alphaproteobacteria genomes found these five regulatory genes nearly universally conserved, absent only in intracellular parasites and members of the order Pelagibacterales, including “Ca. Pelagibacter ubique.” Global differences in mRNA and protein expression between nitrogen-limited and nitrogen-replete cultures were measured to identify nitrogen stress responses in “Ca. Pelagibacter ubique” strain HTCC1062. Transporters for ammonium (AmtB), taurine (TauA), amino acids (YhdW), and opines (OccT) were all elevated in nitrogen-limited cells, indicating that they devote increased resources to the assimilation of nitrogenous organic compounds. Enzymes for assimilating amine into glutamine (GlnA), glutamate (GltBD), and glycine (AspC) were similarly upregulated. Differential regulation of the transcriptional regulator NtrX in the two-component signaling system NtrY/NtrX was also observed, implicating it in control of the nitrogen starvation response. Comparisons of the transcriptome and proteome supported previous observations of uncoupling between transcription and translation in nutrient-deprived “Ca. Pelagibacter ubique” cells. Overall, these data reveal a streamlined, P[subscript II]-independent response to nitrogen stress in “Ca. Pelagibacter ubique,” and likely other Pelagibacterales, and show that they respond to nitrogen stress by allocating more resources to the assimilation of nitrogen-rich organic compounds.
  • This is the publisher’s final pdf. The published article is copyrighted by the author(s) and published by the American Society for Microbiology. The published article can be found at: http://mbio.asm.org/.
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  • Smith DP, Thrash JC, Nicora CD, Lipton MS, Burnum-Johnson KE, Carini P, Smith RD, Giovannoni SJ. 2013. Proteomic and transcriptomic analyses of “Candidatus Pelagibacter ubique” describe the first P[subscript II]-independent response to nitrogen limitation in a free-living alphaproteobacterium. mBio 4(6):e00133-12. doi:10.1128/mBio.00133-12
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  • 4
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  • This study was supported by a Marine Microbiology Initiative investigatoraward (S.J.G.) from the Gordon and Betty Moore Foundation. The phylogenomicsportions of this work (J.C.T.) were supported by the NationalScience Foundation under award no. DBI-1003269. Proteomics measurementswere supported by the U.S. Department of Energy (DOE) Office ofBiological and Environmental Research (OBER) Pan-omics program atPacific Northwest National Laboratory (PNNL) and performed in theEnvironmental Molecular Sciences Laboratory, a DOE OBER nationalscientific user facility on the PNNL campus. PNNL is a multiprogramnational laboratory operated by Battelle for the DOE under contract DE-AC05-76RL01830.
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