title: Transcriptional and translational regulatory responses to iron limitation in the globally distributed marine bacterium Candidatus pelagibacter ubique.
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.
authors.affiliation: Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Daniel P
authors.initials: DP
authors.lastname: Smith
authors.forename: Joshua B
authors.initials: JB
authors.lastname: Kitner
authors.forename: Angela D
authors.initials: AD
authors.lastname: Norbeck
authors.forename: Therese R
authors.initials: TR
authors.lastname: Clauss
authors.forename: Mary S
authors.initials: MS
authors.lastname: Lipton
authors.forename: Michael S
authors.initials: MS
authors.lastname: Schwalbach
authors.forename: Laura
authors.initials: L
authors.lastname: Steindler
authors.forename: Carrie D
authors.initials: CD
authors.lastname: Nicora
authors.forename: Richard D
authors.initials: RD
authors.lastname: Smith
authors.forename: Stephen J
authors.initials: SJ
authors.lastname: Giovannoni
mesh_terms: D020561:Alphaproteobacteria / Q000166:cytology / Q000187:drug effects* / Q000235:genetics*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D049109:Cell Proliferation / Q000187:drug effects; D003080:Cold Temperature; D015964:Gene Expression Regulation, Bacterial / Q000187:drug effects; D005798:Genes, Bacterial / Q000235:genetics; D007501:Iron / Q000494:pharmacology; D000090463:Iron Deficiencies; D020411:Oligonucleotide Array Sequence Analysis; D014176:Protein Biosynthesis / Q000187:drug effects; D040901:Proteomics; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012623:Seawater / Q000382:microbiology*; D017262:Siderophores / Q000378:metabolism; D014158:Transcription, Genetic / Q000187:drug effects
chemical_list: D001426:Bacterial Proteins; D012333:RNA, Messenger; D017262:Siderophores; D007501:Iron
references.citation: Appl Environ Microbiol. 2008 Jul;74(13):4091-100
references.pmid: 18469119
references.citation: Environ Microbiol. 2009 Jan;11(1):230-8
references.pmid: 19125817
references.citation: Science. 2001 May 4;292(5518):929-34
references.pmid: 11340206
references.citation: J Bacteriol. 2005 Jul;187(14):4865-74
references.pmid: 15995201
references.citation: FEBS Lett. 2005 Oct 24;579(25):5454-60
references.pmid: 16212958
references.citation: PLoS Comput Biol. 2006 Dec 15;2(12):e163
references.pmid: 17173478
references.citation: Curr Opin Microbiol. 2000 Apr;3(2):149-53
references.pmid: 10745002
references.citation: J Biol Chem. 2003 Oct 3;278(40):38395-401
references.pmid: 12881516
references.citation: EMBO J. 2007 Feb 21;26(4):965-75
references.pmid: 17268550
references.citation: Science. 2005 Aug 19;309(5738):1242-5
references.pmid: 16109880
references.citation: Appl Environ Microbiol. 2004 Jul;70(7):4129-35
references.pmid: 15240292
references.citation: Biol Chem. 2008 May;389(5):585-98
references.pmid: 18953726
references.citation: Anal Chem. 2006 Nov 15;78(22):7796-801
references.pmid: 17105173
references.citation: Biochem Soc Trans. 2008 Oct;36(Pt 5):1088-90
references.pmid: 18793194
references.citation: Appl Environ Microbiol. 2005 Jun;71(6):2979-86
references.pmid: 15932993
references.citation: Arch Microbiol. 2002 Jun;177(6):433-40
references.pmid: 12029388
references.citation: J Bacteriol. 2001 Feb;183(4):1205-14
references.pmid: 11157932
references.citation: Mol Cell Proteomics. 2002 Apr;1(4):304-13
references.pmid: 12096112
references.citation: Nature. 2000 Oct 12;407(6805):695-702
references.pmid: 11048709
references.citation: Mol Microbiol. 2001 Apr;40(1):179-88
references.pmid: 11298285
references.citation: Mol Microbiol. 2006 Apr;60(2):427-37
references.pmid: 16573691
references.citation: J Bacteriol. 2003 Nov;185(21):6348-57
references.pmid: 14563870
references.citation: BMC Genomics. 2009 Jun 16;10:268
references.pmid: 19531245
references.citation: Appl Environ Microbiol. 2002 Aug;68(8):3878-85
references.pmid: 12147485
references.citation: Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7784-9
references.pmid: 10884409
references.citation: Genome Res. 2004 Nov;14(11):2308-18
references.pmid: 15520293
references.citation: J Bacteriol. 1999 Oct;181(20):6223-9
references.pmid: 10515908
references.citation: J Biol Chem. 2005 Mar 4;280(9):7671-6
references.pmid: 15613477
references.citation: J Bacteriol. 2002 Nov;184(21):5826-32
references.pmid: 12374814
references.citation: Microbiology (Reading). 2005 Oct;151(Pt 10):3427-3433
references.pmid: 16207924
references.citation: Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9542-7
references.pmid: 12883001
references.citation: Genome Biol. 2005;6(8):R70
references.pmid: 16086852
references.citation: RNA Biol. 2009 Apr-Jun;6(2):153-60
references.pmid: 19885993
references.citation: J Bacteriol. 2000 Jul;182(13):3802-8
references.pmid: 10850997
references.citation: Genetics. 1996 Aug;143(4):1521-32
references.pmid: 8844142
references.citation: Trends Biochem Sci. 2005 Aug;30(8):462-8
references.pmid: 15996868
references.citation: J Proteome Res. 2006 Feb;5(2):277-86
references.pmid: 16457593
references.citation: Curr Microbiol. 2008 Jul;57(1):18-22
references.pmid: 18363056
references.citation: Nature. 2002 Dec 19-26;420(6917):806-10
references.pmid: 12490947
references.citation: BMC Genomics. 2007 Apr 09;8:96
references.pmid: 17419876
references.citation: Science. 2009 Apr 10;324(5924):255-8
references.pmid: 19359587
references.citation: FEBS J. 2005 Sep;272(18):4691-702
references.pmid: 16156790
references.citation: Mol Biosyst. 2009 Dec;5(12):1512-26
references.pmid: 20023718
references.citation: Curr Opin Microbiol. 2007 Apr;10(2):140-5
references.pmid: 17383226
references.citation: Methods Enzymol. 2003;371:460-71
references.pmid: 14712721
references.citation: Mol Microbiol. 1999 Sep;33(5):1004-14
references.pmid: 10476034
references.citation: Crit Rev Biotechnol. 2007 Apr-Jun;27(2):63-75
references.pmid: 17578703
references.citation: J Bacteriol. 2006 Jan;188(2):733-44
references.pmid: 16385063
references.citation: FEMS Microbiol Rev. 2003 Jun;27(2-3):215-37
references.pmid: 12829269
references.citation: J Biol Chem. 1998 Aug 21;273(34):21669-74
references.pmid: 9705301
references.citation: Mol Cell Proteomics. 2002 Apr;1(4):323-33
references.pmid: 12096114
references.citation: Cell Mol Life Sci. 2006 Mar;63(5):591-600
references.pmid: 16465450
references.citation: J Bacteriol. 2003 Apr;185(7):2194-202
references.pmid: 12644489
references.citation: Science. 2005 Apr 1;308(5718):67-71
references.pmid: 15802595
references.citation: Science. 2009 Apr 10;324(5924):268-72
references.pmid: 19359590
references.citation: Nature. 2002 Oct 31;419(6910):952-6
references.pmid: 12410317
references.citation: Trends Biochem Sci. 1998 Aug;23(8):286-90
references.pmid: 9757828
references.citation: Nature. 2002 Aug 8;418(6898):630-3
references.pmid: 12167859
references.citation: Nature. 1996 Oct 10;383(6600):495 - 501
references.pmid: 18680864
references.citation: Cell Mol Life Sci. 2002 Nov;59(11):1902-13
references.pmid: 12530521
references.citation: Ann Rev Mar Sci. 2009;1:43-63
references.pmid: 21141029
references.citation: Proc Natl Acad Sci U S A. 2008 Aug 19;105(33):11927-32
references.pmid: 18697947
references.citation: Environ Microbiol. 2010 Feb;12(2):490-500
references.pmid: 19889000
references.citation: Mol Microbiol. 1995 Mar;15(6):1081-93
references.pmid: 7623664
references.citation: Acc Chem Res. 2005 Mar;38(3):167-75
references.pmid: 15766235
references.citation: ISME J. 2009 Jan;3(1):93-105
references.pmid: 18769456