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Transcriptional and translational regulatory responses to iron limitation in the globally distributed marine bacterium Candidatus pelagibacter ubique.

Smith DP, Kitner JB, Norbeck AD, Clauss TR, Lipton MS, Schwalbach MS, Steindler L, Nicora CD, Smith RD, Giovannoni SJ - PLoS ONE (2010)

Bottom Line: The marked proteome reduction was not directly correlated to changes in the transcriptome, implicating post-transcriptional regulatory mechanisms as modulators of protein expression.Two RNA-binding proteins, CspE and CspL, correlated well with iron availability, suggesting that they may contribute to the observed differences between the transcriptome and proteome.We propose a model in which the RNA-binding activity of CspE and CspL selectively enables protein synthesis of the iron acquisition protein SfuC during transient growth-limiting episodes of iron scarcity.

View Article: PubMed Central - PubMed

Affiliation: Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Iron is recognized as an important micronutrient that limits microbial plankton productivity over vast regions of the oceans. We investigated the gene expression responses of Candidatus Pelagibacter ubique cultures to iron limitation in natural seawater media supplemented with a siderophore to chelate iron. Microarray data indicated transcription of the periplasmic iron binding protein sfuC increased by 16-fold, and iron transporter subunits, iron-sulfur center assembly genes, and the putative ferroxidase rubrerythrin transcripts increased to a lesser extent. Quantitative peptide mass spectrometry revealed that sfuC protein abundance increased 27-fold, despite an average decrease of 59% across the global proteome. Thus, we propose sfuC as a marker gene for indicating iron limitation in marine metatranscriptomic and metaproteomic ecological surveys. The marked proteome reduction was not directly correlated to changes in the transcriptome, implicating post-transcriptional regulatory mechanisms as modulators of protein expression. Two RNA-binding proteins, CspE and CspL, correlated well with iron availability, suggesting that they may contribute to the observed differences between the transcriptome and proteome. We propose a model in which the RNA-binding activity of CspE and CspL selectively enables protein synthesis of the iron acquisition protein SfuC during transient growth-limiting episodes of iron scarcity.

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Translation of Ca. Pelagibacter ubique's cold shock and iron-binding genes are influenced by iron availability.The abundance of two Ca. Pelagibacter ubique cold shock proteins, CspE and CspL, and the iron-binding protein SfuC, appear to be correlated with iron availability (p-value of .02, .08, and 3e-79, respectively).
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pone-0010487-g004: Translation of Ca. Pelagibacter ubique's cold shock and iron-binding genes are influenced by iron availability.The abundance of two Ca. Pelagibacter ubique cold shock proteins, CspE and CspL, and the iron-binding protein SfuC, appear to be correlated with iron availability (p-value of .02, .08, and 3e-79, respectively).

Mentions: CspL was significantly more abundant in iron-limited cultures (Figure 4), leading us to closely examine the biological activity of this protein as well as the inversely expressed homolog CspE. The first discovered member of the cold-shock protein (CSP) family, E. coli's CspA, is highly upregulated under cold stress; it is believed to associate with and melt double-stranded RNA complexes as a mechanism to prevent spurious stem loop structures from interfering with transcription and translation [54]–[59]. Despite their homology to CspA, many CSP variants are not cold-inducible, but rather are involved in regulating cellular processes [54], [60]–[62] and can even target their activity to specific RNA sequences [63]. A growing body of literature has described mRNAs which modulate their own expression via temperature- (RNA thermometer) or ligand-sensitive (riboswitch) secondary structures [64], [65]. Due to the episodic nature of iron deposition into ocean surface waters [66] and the resulting selective pressure favoring rapid response systems for this limiting nutrient [67], we speculate that Ca. Pelagibacter ubique CspE and/or CspL affects a reversible inhibition of translation by facilitating an mRNA secondary structure unfavorable for ribosome processing, thereby maintaining the transcriptome in a state of cell growth readiness during times of stress such as iron limitation.


Transcriptional and translational regulatory responses to iron limitation in the globally distributed marine bacterium Candidatus pelagibacter ubique.

Smith DP, Kitner JB, Norbeck AD, Clauss TR, Lipton MS, Schwalbach MS, Steindler L, Nicora CD, Smith RD, Giovannoni SJ - PLoS ONE (2010)

Translation of Ca. Pelagibacter ubique's cold shock and iron-binding genes are influenced by iron availability.The abundance of two Ca. Pelagibacter ubique cold shock proteins, CspE and CspL, and the iron-binding protein SfuC, appear to be correlated with iron availability (p-value of .02, .08, and 3e-79, respectively).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2864753&req=5

pone-0010487-g004: Translation of Ca. Pelagibacter ubique's cold shock and iron-binding genes are influenced by iron availability.The abundance of two Ca. Pelagibacter ubique cold shock proteins, CspE and CspL, and the iron-binding protein SfuC, appear to be correlated with iron availability (p-value of .02, .08, and 3e-79, respectively).
Mentions: CspL was significantly more abundant in iron-limited cultures (Figure 4), leading us to closely examine the biological activity of this protein as well as the inversely expressed homolog CspE. The first discovered member of the cold-shock protein (CSP) family, E. coli's CspA, is highly upregulated under cold stress; it is believed to associate with and melt double-stranded RNA complexes as a mechanism to prevent spurious stem loop structures from interfering with transcription and translation [54]–[59]. Despite their homology to CspA, many CSP variants are not cold-inducible, but rather are involved in regulating cellular processes [54], [60]–[62] and can even target their activity to specific RNA sequences [63]. A growing body of literature has described mRNAs which modulate their own expression via temperature- (RNA thermometer) or ligand-sensitive (riboswitch) secondary structures [64], [65]. Due to the episodic nature of iron deposition into ocean surface waters [66] and the resulting selective pressure favoring rapid response systems for this limiting nutrient [67], we speculate that Ca. Pelagibacter ubique CspE and/or CspL affects a reversible inhibition of translation by facilitating an mRNA secondary structure unfavorable for ribosome processing, thereby maintaining the transcriptome in a state of cell growth readiness during times of stress such as iron limitation.

Bottom Line: The marked proteome reduction was not directly correlated to changes in the transcriptome, implicating post-transcriptional regulatory mechanisms as modulators of protein expression.Two RNA-binding proteins, CspE and CspL, correlated well with iron availability, suggesting that they may contribute to the observed differences between the transcriptome and proteome.We propose a model in which the RNA-binding activity of CspE and CspL selectively enables protein synthesis of the iron acquisition protein SfuC during transient growth-limiting episodes of iron scarcity.

View Article: PubMed Central - PubMed

Affiliation: Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Iron is recognized as an important micronutrient that limits microbial plankton productivity over vast regions of the oceans. We investigated the gene expression responses of Candidatus Pelagibacter ubique cultures to iron limitation in natural seawater media supplemented with a siderophore to chelate iron. Microarray data indicated transcription of the periplasmic iron binding protein sfuC increased by 16-fold, and iron transporter subunits, iron-sulfur center assembly genes, and the putative ferroxidase rubrerythrin transcripts increased to a lesser extent. Quantitative peptide mass spectrometry revealed that sfuC protein abundance increased 27-fold, despite an average decrease of 59% across the global proteome. Thus, we propose sfuC as a marker gene for indicating iron limitation in marine metatranscriptomic and metaproteomic ecological surveys. The marked proteome reduction was not directly correlated to changes in the transcriptome, implicating post-transcriptional regulatory mechanisms as modulators of protein expression. Two RNA-binding proteins, CspE and CspL, correlated well with iron availability, suggesting that they may contribute to the observed differences between the transcriptome and proteome. We propose a model in which the RNA-binding activity of CspE and CspL selectively enables protein synthesis of the iron acquisition protein SfuC during transient growth-limiting episodes of iron scarcity.

Show MeSH
Related in: MedlinePlus