Proteomic and transcriptomic analyses of "Candidatus Pelagibacter ubique" describe the first PII-independent response to nitrogen limitation in a free-living alphaproteobacterium

Daniel P. Smith, J. Cameron Thrash, Carrie D. Nicora, Mary S. Lipton, Kristin E. Burnum-Johnson, Paul Carini, Richard D. Smith, Stephen J. Giovannoni

Research output: Contribution to journalArticlepeer-review

37 Scopus citations

Abstract

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 nutrientdeprived "Ca. Pelagibacter ubique" cells. Overall, these data reveal a streamlined, PII-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.

Original languageEnglish (US)
Article numbere00133-12
JournalmBio
Volume4
Issue number6
DOIs
StatePublished - Nov 26 2013
Externally publishedYes

ASJC Scopus subject areas

  • Microbiology
  • Virology

Fingerprint

Dive into the research topics of 'Proteomic and transcriptomic analyses of "Candidatus Pelagibacter ubique" describe the first PII-independent response to nitrogen limitation in a free-living alphaproteobacterium'. Together they form a unique fingerprint.

Cite this