Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Walworth, Nathan; Pfreundt, Ulrike; Nelson, William C.; Mincer, Tracy; Heidelberg, John F.; Fu, Feixue; Waterbury, John B.; Glavina del Rio, Tijana; Goodwin, Lynne; Kyrpides, Nikos C.; Land, Miriam L.; Woyke, Tanja; Hutchins, David A.; Hess, Wolfgang R.; Webb, Eric A.

doi:10.1073/pnas.1422332112

Title: Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Journal Article · Mon Mar 23 00:00:00 EDT 2015 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1422332112· OSTI ID:1208769

Walworth, Nathan; Pfreundt, Ulrike; Nelson, William C.; Mincer, Tracy; Heidelberg, John F.; Fu, Feixue; Waterbury, John B.; Glavina del Rio, Tijana; Goodwin, Lynne; Kyrpides, Nikos C.; Land, Miriam L.; Woyke, Tanja; Hutchins, David A.; Hess, Wolfgang R.; Webb, Eric A.

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. In this paper, 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. Finally, 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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Contributing Organization:: Univ. of Southern California, Los Angeles, CA (United States); Woods Hole Oceanographic Inst., Woods Hole, MA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231; AC03-76SF00098

OSTI ID:: 1208769

Alternate ID(s):: OSTI ID: 1286733

Report Number(s):: PNNL-SA-108623; KP1601010

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 14; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 33 works

Citation information provided by
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References (80)

The role of variable DNA tandem repeats in bacterial adaptation Zhou, Kai; Aertsen, Abram; Michiels, Chris W. FEMS Microbiology Reviews, Vol. 38, Issue 1 https://doi.org/10.1111/1574-6976.12036	journal	January 2014
Promoter propagation in prokaryotes Matus-Garcia, Mariana; Nijveen, Harm; van Passel, Mark W. J. Nucleic Acids Research, Vol. 40, Issue 20 https://doi.org/10.1093/nar/gks787	journal	August 2012
Non-coding RNAs in marine Synechococcus and their regulation under environmentally relevant stress conditions Gierga, Gregor; Voss, Björn; Hess, Wolfgang R. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2011.215	journal	January 2012
Growth, Nitrogen Fixation, and Spectral Attenuation in Cultivated Trichodesmium Species Prufert-Bebout, Lee; Paerl, Hans W.; Lassen, Carsten Applied and Environmental Microbiology, Vol. 59, Issue 5 https://doi.org/10.1128/AEM.59.5.1367-1375.1993	journal	January 1993
Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium Tripp, H. James; Bench, Shellie R.; Turk, Kendra A. Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08786	journal	February 2010
Bacterial Associations with Marine Oscillatoria sp. (Trichodesmium sp.) Populations: Ecophysiological Implications1 Paerly, Hans W.; Bebout, Brad M.; Prufert, Leslie E. Journal of Phycology, Vol. 25, Issue 4 https://doi.org/10.1111/j.0022-3646.1989.00773.x	journal	December 1989
Novel Metabolic Attributes of the Genus Cyanothece, Comprising a Group of Unicellular Nitrogen-Fixing Cyanobacteria Bandyopadhyay, Anindita; Elvitigala, Thanura; Welsh, Eric mBio, Vol. 2, Issue 5 https://doi.org/10.1128/mBio.00214-11	journal	October 2011
The Challenge of Regulation in a Minimal Photoautotroph: Non-Coding RNAs in Prochlorococcus Steglich, Claudia; Futschik, Matthias E.; Lindell, Debbie PLoS Genetics, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pgen.1000173	journal	August 2008
Regional distributions of nitrogen-fixing bacteria in the Pacific Ocean Church, Matthew J.; Björkman, Karin M.; Karl, David M. Limnology and Oceanography, Vol. 53, Issue 1 https://doi.org/10.4319/lo.2008.53.1.0063	journal	January 2008
Truncated forms of IS911 transposase downregulate transposition Gueguen, Erwan; Rousseau, Philippe; Duval-Valentin, Guy Molecular Microbiology, Vol. 62, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05424.x	journal	November 2006
Complete Genomic Structure of the Bloom-forming Toxic Cyanobacterium Microcystis aeruginosa NIES-843 Kaneko, Takakazu; Nakajima, Nobuyoshi; Okamoto, Shinobu DNA Research, Vol. 14, Issue 6 https://doi.org/10.1093/dnares/dsm026	journal	January 2007
The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle Welsh, E. A.; Liberton, M.; Stockel, J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 39 https://doi.org/10.1073/pnas.0805418105	journal	September 2008
Biocomputational prediction of non-coding RNAs in model cyanobacteria Voß, Björn; Georg, Jens; Schön, Verena BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-123	journal	January 2009
Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean Letelier, Rm; Karl, Dm Marine Ecology Progress Series, Vol. 133 https://doi.org/10.3354/meps133263	journal	January 1996
The fate of nitrogen fixed by diazotrophs in the ocean Mulholland, M. R. Biogeosciences, Vol. 4, Issue 1 https://doi.org/10.5194/bg-4-37-2007	journal	January 2007
Impact of Small Repeat Sequences on Bacterial Genome Evolution Delihas, Nicholas Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr077	journal	January 2011
Molecular assessment of phosphorus and iron physiology in Trichodesmium populations from the western Central and western South Atlantic Webb, Eric A.; Jakuba, Rachel Wisniewski; Moffett, James W. Limnology and Oceanography, Vol. 52, Issue 5 https://doi.org/10.4319/lo.2007.52.5.2221	journal	September 2007
The genomic basis of trophic strategy in marine bacteria Lauro, F. M.; McDougald, D.; Thomas, T. Proceedings of the National Academy of Sciences, Vol. 106, Issue 37, p. 15527-15533 https://doi.org/10.1073/pnas.0903507106	journal	September 2009
Laboratory culture studies of Trichodesmium isolated from the Great Barrier Reef Lagoon, Australia Bell, Peter R. F.; Uwins, Philippa J. R.; Elmetri, Ibrahim Hydrobiologia, Vol. 532, Issue 1-3 https://doi.org/10.1007/s10750-004-8768-1	journal	January 2005
From The Cover: Bacterial genome size reduction by experimental evolution Nilsson, A. I.; Koskiniemi, S.; Eriksson, S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 34 https://doi.org/10.1073/pnas.0503654102	journal	August 2005
The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey Sheridan, C. C. Journal of Plankton Research, Vol. 24, Issue 9 https://doi.org/10.1093/plankt/24.9.913	journal	September 2002
Genome-wide comparison of cyanobacterial transposable elements, potential genetic diversity indicators Lin, Shen; Haas, Stefan; Zemojtel, Tomasz Gene, Vol. 473, Issue 2 https://doi.org/10.1016/j.gene.2010.11.011	journal	March 2011
Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System: SOUTH ATLANTIC N ₂ FIXATION Sohm, Jill A.; Hilton, Jason A.; Noble, Abigail E. Geophysical Research Letters, Vol. 38, Issue 16 https://doi.org/10.1029/2011GL048315	journal	August 2011
ViennaRNA Package 2.0 Lorenz, Ronny; Bernhart, Stephan H.; Höner zu Siederdissen, Christian Algorithms for Molecular Biology, Vol. 6, Issue 1 https://doi.org/10.1186/1748-7188-6-26	journal	November 2011
High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean Montoya, Joseph P.; Holl, Carolyn M.; Zehr, Jonathan P. Nature, Vol. 430, Issue 7003 https://doi.org/10.1038/nature02824	journal	August 2004
Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium Hynes, Annette M.; Chappell, P. Dreux; Dyhrman, Sonya T. Limnology and Oceanography, Vol. 54, Issue 5 https://doi.org/10.4319/lo.2009.54.5.1438	journal	June 2009
Streamlined Regulation and Gene Loss as Adaptive Mechanisms in Prochlorococcus for Optimized Nitrogen Utilization in Oligotrophic Environments Garcia-Fernandez, J. M.; de Marsac, N. T.; Diez, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/MMBR.68.4.630-638.2004	journal	December 2004
A seasonal study of the significance of N2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-series Study (BATS) site Orcutt, Karen M.; Lipschultz, Fredric; Gundersen, Kjell Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 48, Issue 8-9 https://doi.org/10.1016/S0967-0645(00)00157-0	journal	January 2001
Nitrogen fixation by marine cyanobacteria Zehr, Jonathan P. Trends in Microbiology, Vol. 19, Issue 4 https://doi.org/10.1016/j.tim.2010.12.004	journal	April 2011
Secondary Structure Prediction for Aligned RNA Sequences Hofacker, Ivo L.; Fekete, Martin; Stadler, Peter F. Journal of Molecular Biology, Vol. 319, Issue 5 https://doi.org/10.1016/S0022-2836(02)00308-X	journal	June 2002
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean Swan, B. K.; Tupper, B.; Sczyrba, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1304246110	journal	June 2013
Processes and patterns of oceanic nutrient limitation Moore, C. M.; Mills, M. M.; Arrigo, K. R. Nature Geoscience, Vol. 6, Issue 9 https://doi.org/10.1038/ngeo1765	journal	March 2013
Unicellular Cyanobacterial Distributions Broaden the Oceanic N2 Fixation Domain Moisander, P. H.; Beinart, R. A.; Hewson, I. Science, Vol. 327, Issue 5972 https://doi.org/10.1126/science.1185468	journal	February 2010
Deletional bias and the evolution of bacterial genomes Mira, Alex; Ochman, Howard; Moran, Nancy A. Trends in Genetics, Vol. 17, Issue 10 https://doi.org/10.1016/S0168-9525(01)02447-7	journal	October 2001
The consequences of genetic drift for bacterial genome complexity Kuo, C. -H.; Moran, N. A.; Ochman, H. Genome Research, Vol. 19, Issue 8 https://doi.org/10.1101/gr.091785.109	journal	June 2009
Variable Tandem Repeats Accelerate Evolution of Coding and Regulatory Sequences Gemayel, Rita; Vinces, Marcelo D.; Legendre, Matthieu Annual Review of Genetics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-genet-072610-155046	journal	December 2010
Emerging patterns of marine nitrogen fixation Sohm, Jill A.; Webb, Eric A.; Capone, Douglas G. Nature Reviews Microbiology, Vol. 9, Issue 7 https://doi.org/10.1038/nrmicro2594	journal	June 2011
Distribution and activity of diazotrophs in the Eastern Equatorial Atlantic Foster, Rachel A.; Subramaniam, Ajit; Zehr, Jonathan P. Environmental Microbiology, Vol. 11, Issue 4 https://doi.org/10.1111/j.1462-2920.2008.01796.x	journal	April 2009
RNAalifold: improved consensus structure prediction for RNA alignments Bernhart, Stephan H.; Hofacker, Ivo L.; Will, Sebastian BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-474	journal	November 2008
Genesis, effects and fates of repeats in prokaryotic genomes Treangen, Todd J.; Abraham, Anne-Laure; Touchon, Marie FEMS Microbiology Reviews, Vol. 33, Issue 3 https://doi.org/10.1111/j.1574-6976.2009.00169.x	journal	May 2009
Streamlining and Simplification of Microbial Genome Architecture Lynch, Michael Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142300	journal	October 2006
Summer phytoplankton blooms in the oligotrophic North Pacific Subtropical Gyre: Historical perspective and recent observations Dore, John E.; Letelier, Ricardo M.; Church, Matthew J. Progress in Oceanography, Vol. 76, Issue 1 https://doi.org/10.1016/j.pocean.2007.10.002	journal	January 2008
The Nature and Dynamics of Bacterial Genomes Ochman, H. Science, Vol. 311, Issue 5768 https://doi.org/10.1126/science.1119966	journal	March 2006
Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean Hewson, Ian; Poretsky, Rachel S.; Dyhrman, Sonya T. The ISME Journal, Vol. 3, Issue 11 https://doi.org/10.1038/ismej.2009.75	journal	July 2009
Inferring Noncoding RNA Families and Classes by Means of Genome-Scale Structure-Based Clustering Will, Sebastian; Reiche, Kristin; Hofacker, Ivo L. PLoS Computational Biology, Vol. 3, Issue 4 https://doi.org/10.1371/journal.pcbi.0030065	journal	January 2007
Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north Atlantic Ocean Foster, R. A.; Subramaniam, A.; Mahaffey, C. Limnology and Oceanography, Vol. 52, Issue 2 https://doi.org/10.4319/lo.2007.52.2.0517	journal	March 2007
Abundances and Distributions of the Dominant nifH Phylotypes in the Northern Atlantic Ocean Langlois, R. J.; Hummer, D.; LaRoche, J. Applied and Environmental Microbiology, Vol. 74, Issue 6 https://doi.org/10.1128/AEM.01720-07	journal	February 2008
An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea Capone, Dg; Subramaniam, A.; Montoya, Jp Marine Ecology Progress Series, Vol. 172 https://doi.org/10.3354/meps172281	journal	January 1998
Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities Sinha, Rati; Pearson, Leanne A.; Davis, Timothy W. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-83	journal	January 2014
Characterization of Trichodesmium spp. by Genetic Techniques Orcutt, K. M.; Rasmussen, U.; Webb, E. A. Applied and Environmental Microbiology, Vol. 68, Issue 5 https://doi.org/10.1128/AEM.68.5.2236-2245.2002	journal	May 2002
Genome Sequence of Lactobacillus helveticus, an Organism Distinguished by Selective Gene Loss and Insertion Sequence Element Expansion Callanan, M.; Kaleta, P.; O'Callaghan, J. Journal of Bacteriology, Vol. 190, Issue 2 https://doi.org/10.1128/JB.01295-07	journal	November 2007
Characterization of diatom–cyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences Foster, Rachel A.; Zehr, Jonathan P. Environmental Microbiology, Vol. 8, Issue 11 https://doi.org/10.1111/j.1462-2920.2006.01068.x	journal	November 2006
A PCR technique based on the Hipl interspersed repetitive sequence distinguishes cyanobacterial species and strains Smith, J. K.; Parry, J. D.; Day, J. G. Microbiology, Vol. 144, Issue 10 https://doi.org/10.1099/00221287-144-10-2791	journal	October 1998
SAR11 marine bacteria require exogenous reduced sulphur for growth Tripp, H. James; Kitner, Joshua B.; Schwalbach, Michael S. Nature, Vol. 452, Issue 7188 https://doi.org/10.1038/nature06776	journal	March 2008
Two Strains of Crocosphaera watsonii with Highly Conserved Genomes are Distinguished by Strain-Specific Features Bench, Shellie R.; Ilikchyan, Irina N.; Tripp, H. James Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00261	journal	January 2011
Comparative systems biology across an evolutionary gradient within the Shewanella genus Konstantinidis, Konstantinos T.; Serres, Margrethe H.; Romine, Margaret F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 37 https://doi.org/10.1073/pnas.0902000106	journal	September 2009
The frailty of adaptive hypotheses for the origins of organismal complexity Lynch, M. Proceedings of the National Academy of Sciences, Vol. 104, Issue Supplement 1 https://doi.org/10.1073/pnas.0702207104	journal	May 2007
Comparison of Cultured Trichodesmium (Cyanophyceae) with Species Characterized from the Field1: Trichodesmium Characterization Hynes, Annette M.; Webb, Eric A.; Doney, Scott C. Journal of Phycology, Vol. 48, Issue 1 https://doi.org/10.1111/j.1529-8817.2011.01096.x	journal	December 2011
Environmental Genome Shotgun Sequencing of the Sargasso Sea Venter, J. C. Science, Vol. 304, Issue 5667 https://doi.org/10.1126/science.1093857	journal	April 2004
Whole genome comparison of six Crocosphaera watsonii strains with differing phenotypes Bench, Shellie R.; Heller, Philip; Frank, Ildiko Journal of Phycology, Vol. 49, Issue 4 https://doi.org/10.1111/jpy.12090	journal	July 2013
Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre: N Church, Matthew J.; Mahaffey, Claire; Letelier, Ricardo M. Global Biogeochemical Cycles, Vol. 23, Issue 2 https://doi.org/10.1029/2008GB003418	journal	June 2009
Genome Streamlining in a Cosmopolitan Oceanic Bacterium Giovannoni, S. J. Science, Vol. 309, Issue 5738 https://doi.org/10.1126/science.1114057	journal	August 2005
The primary transcriptome of the marine diazotroph Trichodesmium erythraeum IMS101 Pfreundt, Ulrike; Kopf, Matthias; Belkin, Natalia Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06187	journal	August 2014
Unicellular Cyanobacterium Symbiotic with a Single-Celled Eukaryotic Alga Thompson, A. W.; Foster, R. A.; Krupke, A. Science, Vol. 337, Issue 6101 https://doi.org/10.1126/science.1222700	journal	September 2012
Amazon River enhances diazotrophy and carbon sequestration in the tropical North Atlantic Ocean Subramaniam, A.; Yager, P. L.; Carpenter, E. J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 30 https://doi.org/10.1073/pnas.0710279105	journal	July 2008
Characterization of bacterial epibionts on the cyanobacterium Trichodesmium Hmelo, Lr; Van Mooy, Bas; Mincer, Tj Aquatic Microbial Ecology, Vol. 67, Issue 1 https://doi.org/10.3354/ame01571	journal	July 2012
Patterns and Implications of Gene Gain and Loss in the Evolution of Prochlorococcus Kettler, Gregory C.; Martiny, Adam C.; Huang, Katherine PLoS Genetics, Vol. 3, Issue 12 https://doi.org/10.1371/journal.pgen.0030231	journal	January 2007
Spatial and temporal distribution of Trichodesmium spp. in the stratified Gulf of Aqaba, Red Sea Post, Af; Dedej, Z.; Gottlieb, R. Marine Ecology Progress Series, Vol. 239 https://doi.org/10.3354/meps239241	journal	January 2002
Bacterial insertion sequences: their genomic impact and diversity Siguier, Patricia; Gourbeyre, Edith; Chandler, Mick FEMS Microbiology Reviews, Vol. 38, Issue 5 https://doi.org/10.1111/1574-6976.12067	journal	September 2014
Doubling of marine dinitrogen-fixation rates based on direct measurements Großkopf, Tobias; Mohr, Wiebke; Baustian, Tina Nature, Vol. 488, Issue 7411 https://doi.org/10.1038/nature11338	journal	August 2012
Ecological Genomics of Marine Picocyanobacteria Scanlan, D. J.; Ostrowski, M.; Mazard, S. Microbiology and Molecular Biology Reviews, Vol. 73, Issue 2 https://doi.org/10.1128/MMBR.00035-08	journal	June 2009
The Origins of Genome Complexity Lynch, Michael; Conery, John S. Science, Vol. 302, Issue 5649 https://doi.org/10.1126/science.1089370	journal	November 2003
In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii Hewson, Ian; Poretsky, Rachel S.; Beinart, Roxanne A. The ISME Journal, Vol. 3, Issue 5 https://doi.org/10.1038/ismej.2009.8	journal	February 2009
Trichodesmium, a Globally Significant Marine Cyanobacterium Capone, D. G. Science, Vol. 276, Issue 5316 https://doi.org/10.1126/science.276.5316.1221	journal	May 1997
Denitrifying Alphaproteobacteria from the Arabian Sea That Express nosZ , the Gene Encoding Nitrous Oxide Reductase, in Oxic and Suboxic Waters Wyman, Michael; Hodgson, Sylvia; Bird, Clare Applied and Environmental Microbiology, Vol. 79, Issue 8 https://doi.org/10.1128/AEM.03705-12	journal	February 2013
Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation Karl, D. M.; Church, M. J.; Dore, J. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 6 https://doi.org/10.1073/pnas.1120312109	journal	January 2012
Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation Rocap, Gabrielle; Larimer, Frank W.; Lamerdin, Jane Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01947	journal	August 2003
The genome of a motile marine Synechococcus Palenik, B.; Brahamsha, B.; Larimer, F. W. Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01943	journal	August 2003
Biogeochemical Controls and Feedbacks on Ocean Primary Production Falkowski, P. G. Science, Vol. 281, Issue 5374 https://doi.org/10.1126/science.281.5374.200	journal	July 1998
Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage Dupont, Chris L.; Rusch, Douglas B.; Yooseph, Shibu The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.189	journal	December 2011

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Regulatory RNAs in photosynthetic cyanobacteria Kopf, Matthias; Hess, Wolfgang R. FEMS Microbiology Reviews, Vol. 39, Issue 3 https://doi.org/10.1093/femsre/fuv017	journal	April 2015
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59 BASIC BIOLOGICAL SCIENCES
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evolution genomics
nitrogen fixation

Title: Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

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