title: Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle.
abstract: Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance because of its critical role in oceanic biogeochemistry and primary production. Unlike the other >150 available genomes of free-living cyanobacteria, only 63.8% of the Trichodesmium erythraeum (strain IMS101) genome is predicted to encode protein, which is 20-25% less than the average for other cyanobacteria and nonpathogenic, free-living bacteria. We use distinctive isolates and metagenomic data to show that low coding density observed in IMS101 is a common feature of the Trichodesmium genus, both in culture and in situ. Transcriptome analysis indicates that 86% of the noncoding space is expressed, although the function of these transcripts is unclear. The density of noncoding, possible regulatory elements predicted in Trichodesmium, when normalized per intergenic kilobase, was comparable and twofold higher than that found in the gene-dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium noncoding RNA secondary structures were predicted between most culture and metagenomic sequences, lending support to the structural conservation. Conservation of these intergenic regions in spatiotemporally separated Trichodesmium populations suggests possible genus-wide selection for their maintenance. These large intergenic spacers may have developed during intervals of strong genetic drift caused by periodic blooms of a subset of genotypes, which may have reduced effective population size. Our data suggest that transposition of selfish DNA, low effective population size, and high-fidelity replication allowed the unusual "inflation" of noncoding sequence observed in Trichodesmium despite its oligotrophic lifestyle.
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
authors.forename: Nathan
authors.initials: N
authors.lastname: Walworth
authors.affiliation: Genetics and Experiment Bioinformatics, University of Freiburg, 79098 Freiburg, Germany;
authors.forename: Ulrike
authors.initials: U
authors.lastname: Pfreundt
authors.affiliation: Fundamental and Computational Sciences, Pacific Northwest National Laboratory, Richland, WA 99352;
authors.forename: William C
authors.initials: WC
authors.lastname: Nelson
authors.affiliation: Marine Chemistry and Geochemistry Department and.
authors.forename: Tracy
authors.initials: T
authors.lastname: Mincer
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
authors.forename: John F
authors.initials: JF
authors.lastname: Heidelberg
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
authors.forename: Feixue
authors.initials: F
authors.lastname: Fu
authors.affiliation: Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543;
authors.forename: John B
authors.initials: JB
authors.lastname: Waterbury
authors.affiliation: Joint Genome Institute, Walnut Creek, CA 94598; and.
authors.forename: Tijana
authors.initials: T
authors.lastname: Glavina del Rio
authors.affiliation: Joint Genome Institute, Walnut Creek, CA 94598; and.
authors.forename: Lynne
authors.initials: L
authors.lastname: Goodwin
authors.affiliation: Joint Genome Institute, Walnut Creek, CA 94598; and.
authors.forename: Nikos C
authors.initials: NC
authors.lastname: Kyrpides
authors.affiliation: Oak Ridge National Laboratory, Oak Ridge, TN 37831.
authors.forename: Miriam L
authors.initials: ML
authors.lastname: Land
authors.affiliation: Joint Genome Institute, Walnut Creek, CA 94598; and.
authors.forename: Tanja
authors.initials: T
authors.lastname: Woyke
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
authors.forename: David A
authors.initials: DA
authors.lastname: Hutchins
authors.affiliation: Genetics and Experiment Bioinformatics, University of Freiburg, 79098 Freiburg, Germany;
authors.forename: Wolfgang R
authors.initials: WR
authors.lastname: Hess
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089; eawebb@usc.edu.
authors.forename: Eric A
authors.initials: EA
authors.lastname: Webb
mesh_terms: D001426:Bacterial Proteins / Q000737:chemistry; D002244:Carbon / Q000737:chemistry; D019295:Computational Biology; D000458:Cyanobacteria / Q000235:genetics* / Q000502:physiology*; D004269:DNA, Bacterial / Q000737:chemistry* / Q000235:genetics; D021901:DNA, Intergenic / Q000235:genetics; D017753:Ecosystem; D015964:Gene Expression Regulation, Bacterial; D005798:Genes, Bacterial; D016678:Genome; D023281:Genomics; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000737:chemistry; D009586:Nitrogen Fixation / Q000235:genetics; D009690:Nucleic Acid Conformation; D009792:Oceans and Seas; D048929:Prochlorococcus / Q000235:genetics; D012313:RNA / Q000737:chemistry / Q000235:genetics; D015398:Signal Transduction; D046940:Synechococcus / Q000235:genetics; D019895:Transposases / Q000378:metabolism
chemical_list: D001426:Bacterial Proteins; D004269:DNA, Bacterial; D021901:DNA, Intergenic; D012313:RNA; D002244:Carbon; D019895:Transposases; D009584:Nitrogen
keywords: evolution genomics; marine microbiology; nitrogen fixation; oligotrophic
references.citation: Trends Genet. 2001 Oct;17(10):589-96
references.pmid: 11585665
references.citation: Appl Environ Microbiol. 2002 May;68(5):2236-45
references.pmid: 11976093
references.citation: J Mol Biol. 2002 Jun 21;319(5):1059-66
references.pmid: 12079347
references.citation: Nature. 2003 Aug 28;424(6952):1037-42
references.pmid: 12917641
references.citation: Nature. 2003 Aug 28;424(6952):1042-7
references.pmid: 12917642
references.citation: Science. 2003 Nov 21;302(5649):1401-4
references.pmid: 14631042
references.citation: Science. 2004 Apr 2;304(5667):66-74
references.pmid: 15001713
references.citation: Nature. 2004 Aug 26;430(7003):1027-32
references.pmid: 15329721
references.citation: Microbiol Mol Biol Rev. 2004 Dec;68(4):630-8
references.pmid: 15590777
references.citation: Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12112-6
references.pmid: 16099836
references.citation: Science. 2005 Aug 19;309(5738):1242-5
references.pmid: 16109880
references.citation: Appl Environ Microbiol. 1993 May;59(5):1367-75
references.pmid: 16348931
references.citation: Science. 2006 Mar 24;311(5768):1730-3
references.pmid: 16556833
references.citation: Annu Rev Microbiol. 2006;60:327-49
references.pmid: 16824010
references.citation: Environ Microbiol. 2006 Nov;8(11):1913-25
references.pmid: 17014491
references.citation: Mol Microbiol. 2006 Nov;62(4):1102-16
references.pmid: 17078817
references.citation: PLoS Comput Biol. 2007 Apr 13;3(4):e65
references.pmid: 17432929
references.citation: Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8597-604
references.pmid: 17494740
references.citation: J Bacteriol. 2008 Jan;190(2):727-35
references.pmid: 17993529
references.citation: PLoS Genet. 2007 Dec;3(12):e231
references.pmid: 18159947
references.citation: DNA Res. 2007 Dec 31;14(6):247-56
references.pmid: 18192279
references.citation: Appl Environ Microbiol. 2008 Mar;74(6):1922-31
references.pmid: 18245263
references.citation: Nature. 2008 Apr 10;452(7188):741-4
references.pmid: 18337719
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10460-5
references.pmid: 18647838
references.citation: PLoS Genet. 2008 Aug 29;4(8):e1000173
references.pmid: 18769676
references.citation: Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15094-9
references.pmid: 18812508
references.citation: BMC Bioinformatics. 2008 Nov 11;9:474
references.pmid: 19014431
references.citation: Environ Microbiol. 2009 Apr;11(4):741-50
references.pmid: 19175790
references.citation: ISME J. 2009 May;3(5):618-31
references.pmid: 19225552
references.citation: BMC Genomics. 2009 Mar 23;10:123
references.pmid: 19309518
references.citation: FEMS Microbiol Rev. 2009 May;33(3):539-71
references.pmid: 19396957
references.citation: Microbiol Mol Biol Rev. 2009 Jun;73(2):249-99
references.pmid: 19487728
references.citation: Genome Res. 2009 Aug;19(8):1450-4
references.pmid: 19502381
references.citation: ISME J. 2009 Nov;3(11):1286-300
references.pmid: 19571897
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15527-33
references.pmid: 19805210
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15909-14
references.pmid: 19805231
references.citation: Nature. 2010 Mar 4;464(7285):90-4
references.pmid: 20173737
references.citation: Science. 2010 Mar 19;327(5972):1512-4
references.pmid: 20185682
references.citation: Annu Rev Genet. 2010;44:445-77
references.pmid: 20809801
references.citation: Gene. 2011 Mar 1;473(2):139-49
references.pmid: 21156198
references.citation: Trends Microbiol. 2011 Apr;19(4):162-73
references.pmid: 21227699
references.citation: Nat Rev Microbiol. 2011 Jun 16;9(7):499-508
references.pmid: 21677685
references.citation: Genome Biol Evol. 2011;3:959-73
references.pmid: 21803768
references.citation: MBio. 2011 Oct 04;2(5):null
references.pmid: 21972240
references.citation: Algorithms Mol Biol. 2011 Nov 24;6:26
references.pmid: 22115189
references.citation: ISME J. 2012 Jun;6(6):1186-99
references.pmid: 22170421
references.citation: Front Microbiol. 2011 Dec 29;2:261
references.pmid: 22232617
references.citation: ISME J. 2012 Aug;6(8):1544-57
references.pmid: 22258101
references.citation: Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):1842-9
references.pmid: 22308450
references.citation: MBio. 2012 May 02;3(2):null
references.pmid: 22448042
references.citation: Nature. 2012 Aug 16;488(7411):361-4
references.pmid: 22878720
references.citation: Nucleic Acids Res. 2012 Nov 1;40(20):10032-40
references.pmid: 22933716
references.citation: Science. 2012 Sep 21;337(6101):1546-50
references.pmid: 22997339
references.citation: Appl Environ Microbiol. 2013 Apr;79(8):2670-81
references.pmid: 23396348
references.citation: Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11463-8
references.pmid: 23801761
references.citation: FEMS Microbiol Rev. 2014 Jan;38(1):119-41
references.pmid: 23927439
references.citation: BMC Genomics. 2014 Jan 29;15:83
references.pmid: 24476316
references.citation: FEMS Microbiol Rev. 2014 Sep;38(5):865-91
references.pmid: 24499397
references.citation: Sci Rep. 2014 Aug 26;4:6187
references.pmid: 25155278
references.citation: J Phycol. 2013 Aug;49(4):786-801
references.pmid: 27007210
references.citation: J Phycol. 2012 Feb;48(1):196-210
references.pmid: 27009664
references.citation: Science. 1998 Jul 10;281(5374):200-7
references.pmid: 9660741
references.citation: Microbiology. 1998 Oct;144 ( Pt 10):2791-801
references.pmid: 9802020