Proteome Remodeling in Response to Sulfur Limitation in “ Candidatus Pelagibacter ubique”

Smith, Daniel P.; Nicora, Carrie D.; Carini, Paul; Lipton, Mary S.; Norbeck, Angela D.; Smith, Richard D.; Giovannoni, Stephen J.; Wilmes, ed., Paul

doi:10.1128/mSystems.00068-16

Title: Proteome Remodeling in Response to Sulfur Limitation in “ Candidatus Pelagibacter ubique”

Journal Article · Tue Aug 30 00:00:00 EDT 2016 · mSystems

DOI:https://doi.org/10.1128/mSystems.00068-16· OSTI ID:1618364

Smith, Daniel P. ^[1]; Nicora, Carrie D. ^[2]; Carini, Paul ^[1]; Lipton, Mary S. ^[2]; Norbeck, Angela D. ^[2]; Smith, Richard D. ^[2]; Giovannoni, Stephen J. ^[1]; Wilmes, ed., Paul

Department of Microbiology, Oregon State University, Corvallis, Oregon, USA
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA

“ Ca . Pelagibacter ubique” is a key driver of marine biogeochemistry cycles and a model for understanding how minimal genomes evolved in free-living anucleate organisms. This study explores the unusual sulfur acquisition strategy that has evolved in these cells, which lack assimilatory sulfate reduction and instead rely on reduced sulfur compounds found in oxic marine environments to meet their cellular quotas. Our findings demonstrate that the sulfur acquisition systems are constitutively expressed but the enzymatic steps leading to the essential sulfur-containing amino acid methionine are regulated by a unique array of riboswitches and genes, many of which are encoded in a rapidly evolving genome region. These findings support mounting evidence that streamlined cells have evolved regulatory mechanisms that minimize transcriptional switching and, unexpectedly, localize essential sulfur acquisition genes in a genome region normally associated with adaption to environmental variation.

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Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1618364

Journal Information:: mSystems, Journal Name: mSystems Vol. 1 Journal Issue: 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 13 works

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References (88)

Global Regulation of the Response to Sulfur Availability in the Cheese-Related Bacterium Brevibacterium aurantiacum Forquin, Marie-Pierre; Hébert, Agnès; Roux, Aurélie Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.01708-10	journal	December 2010
Dimethylsulfoniopropionate Uptake by Marine Phytoplankton Vila-Costa, M.; Simo, R.; Harada, H. Science, Vol. 314, Issue 5799 https://doi.org/10.1126/science.1131043	journal	October 2006
Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments Gonzalez, J. M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 5 https://doi.org/10.1099/ijs.0.02491-0	journal	September 2003
A global response to sulfur starvation in Pseudomonas putida and its relationship to the expression of low-sulfur-content proteins Scott, Colin; Hilton, Margaret E.; Coppin, Christopher W. FEMS Microbiology Letters, Vol. 267, Issue 2 https://doi.org/10.1111/j.1574-6968.2006.00575.x	journal	February 2007
Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico Malmstrom, Rex R.; Kiene, Ronald P.; Kirchman, David L. Limnology and Oceanography, Vol. 49, Issue 2 https://doi.org/10.4319/lo.2004.49.2.0597	journal	March 2004
Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data Wilhelm, Larry J.; Tripp, H. James; Givan, Scott A. Biology Direct, Vol. 2, Issue 1 https://doi.org/10.1186/1745-6150-2-27	journal	January 2007
Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic Simó, Rafel; Archer, Stephen D.; Pedrós-Alió, Carlos Limnology and Oceanography, Vol. 47, Issue 1 https://doi.org/10.4319/lo.2002.47.1.0053	journal	January 2002
The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol Sun, Jing; Todd, Jonathan D.; Thrash, J. Cameron Nature Microbiology, Vol. 1, Issue 8 https://doi.org/10.1038/nmicrobiol.2016.65	journal	May 2016
The structure of Desulfovibrio vulgaris rubrerythrin reveals a unique combination of rubredoxin-like FeS4 and ferritin-like diiron domains deMaré, Fredrick; Kurtz, Donald M.; Nordlund, Pär Nature Structural & Molecular Biology, Vol. 3, Issue 6 https://doi.org/10.1038/nsb0696-539	journal	June 1996
Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process Hill, Rw; White, Ba; Cottrell, Mt Aquatic Microbial Ecology, Vol. 14 https://doi.org/10.3354/ame014001	journal	January 1998
Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803 Zhang, Zhigang; Pendse, Ninad D.; Phillips, Katherine N. BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-344	journal	January 2008
Genomic Islands and the Ecology and Evolution of Prochlorococcus Coleman, M. L. Science, Vol. 311, Issue 5768 https://doi.org/10.1126/science.1122050	journal	March 2006
Homology Modeling of Dissimilatory APS Reductases (AprBA) of Sulfur-Oxidizing and Sulfate-Reducing Prokaryotes Meyer, Birte; Kuever, Jan PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001514	journal	January 2008
Purification, Kinetic Properties, and cDNA Cloning of Mammalian Betaine-Homocysteine Methyltransferase Garrow, Timothy A. Journal of Biological Chemistry, Vol. 271, Issue 37 https://doi.org/10.1074/jbc.271.37.22831	journal	September 1996
Proteomic Analysis of Stationary Phase in the Marine Bacterium "Candidatus Pelagibacter ubique" Sowell, S. M.; Norbeck, A. D.; Lipton, M. S. Applied and Environmental Microbiology, Vol. 74, Issue 13 https://doi.org/10.1128/AEM.00599-08	journal	May 2008
Dimethylsulfoniopropionate-Dependent Demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi Reisch, Chris R.; Moran, Mary Ann; Whitman, William B. Journal of Bacteriology, Vol. 190, Issue 24 https://doi.org/10.1128/JB.00770-08	journal	October 2008
Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis: Insertional inactivation of P. gingivalis rubreryythrin Sztukowska, Maryta; Bugno, Marcin; Potempa, Jan Molecular Microbiology, Vol. 44, Issue 2 https://doi.org/10.1046/j.1365-2958.2002.02892.x	journal	April 2002
Vienna RNA secondary structure server Hofacker, I. L. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg599	journal	July 2003
The Global Regulator Spx Functions in the Control of Organosulfur Metabolism in Bacillus subtilis Choi, Soon-Yong; Reyes, Dindo; Leelakriangsak, Montira Journal of Bacteriology, Vol. 188, Issue 16 https://doi.org/10.1128/JB.00443-06	journal	August 2006
A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria Poiata, E.; Meyer, M. M.; Ames, T. D. RNA, Vol. 15, Issue 11 https://doi.org/10.1261/rna.1824209	journal	September 2009
The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP Kiene, Ronald P.; Linn, Laura J. Geochimica et Cosmochimica Acta, Vol. 64, Issue 16 https://doi.org/10.1016/S0016-7037(00)00399-9	journal	August 2000
Towards methionine overproduction in Corynebacterium glutamicum - methanethiol and dimethyldisulfide as reduced sulfur sources Bolten, Christoph Joseph JOURNAL OF MICROBIOLOGY AND BIOTECHNOLOGY, Vol. 20, Issue 8 https://doi.org/10.4014/jmb.1002.02018	journal	August 2010
Physiological aspects of the production and conversion of DMSP in marine algae and higher plants Stefels, J. Journal of Sea Research, Vol. 43, Issue 3-4, p. 183-197 https://doi.org/10.1016/S1385-1101(00)00030-7	journal	August 2000
New and important roles for DMSP in marine microbial communities Kiene, R. P.; Linn, L. J.; Bruton, J. A. Journal of Sea Research, Vol. 43, Issue 3-4 https://doi.org/10.1016/S1385-1101(00)00023-X	journal	August 2000
The ß-dimethylsulphoniopropionate (DMSP) Content of Macroalgae from Antarctica and Southern Chile Karsten, U.; Wiencke, C.; Kirst, G. O. Botanica Marina, Vol. 33, Issue 2 https://doi.org/10.1515/botm.1990.33.2.143	journal	January 1990
Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium Carini, Paul; Steindler, Laura; Beszteri, Sara The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.122	journal	October 2012
The I-TASSER Suite: protein structure and function prediction Yang, Jianyi; Yan, Renxiang; Roy, Ambrish Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3213	journal	December 2014
Dimethylsulfoniopropionate: Its Sources, Role in the Marine Food Web, and Biological Degradation to Dimethylsulfide Yoch, D. C. Applied and Environmental Microbiology, Vol. 68, Issue 12 https://doi.org/10.1128/AEM.68.12.5804-5815.2002	journal	December 2002
Bacterial Taxa That Limit Sulfur Flux from the Ocean Howard, E. C.; Henriksen, J. R.; Buchan, A. Science, Vol. 314, Issue 5799 https://doi.org/10.1126/science.1130657	journal	October 2006
Physical Interaction of CcmC with Heme and the Heme Chaperone CcmE during Cytochrome c Maturation Ren, Qun; Thöny-Meyer, Linda Journal of Biological Chemistry, Vol. 276, Issue 35 https://doi.org/10.1074/jbc.M103058200	journal	May 2001
Functional Demonstration of Reverse Transsulfuration in the Mycobacterium tuberculosis Complex Reveals That Methionine Is the Preferred Sulfur Source for Pathogenic Mycobacteria Wheeler, Paul R.; Coldham, Nicholas G.; Keating, Lisa Journal of Biological Chemistry, Vol. 280, Issue 9 https://doi.org/10.1074/jbc.M412540200	journal	December 2004
Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments Kempf, Bettina; Bremer, E. Archives of Microbiology, Vol. 170, Issue 5 https://doi.org/10.1007/s002030050649	journal	September 1998
Identification of cyanobacterial non-coding RNAs by comparative genome analysis Axmann, Ilka M.; Kensche, Philip; Vogel, Jörg Genome Biology, Vol. 6, Issue 9, p. R73 https://doi.org/10.1186/gb-2005-6-9-r73	journal	January 2005
Evidence of a Large Novel Gene Pool Associated with Prokaryotic Genomic Islands Hsiao, William W. L.; Ung, Korine; Aeschliman, Dana PLoS Genetics, Vol. 1, Issue 5 https://doi.org/10.1371/journal.pgen.0010062	journal	November 2005
Transformation of Sulfur Compounds by an Abundant Lineage of Marine Bacteria in the α-Subclass of the ClassProteobacteria González, José M.; Kiene, Ronald P.; Moran, Mary Ann Applied and Environmental Microbiology, Vol. 65, Issue 9 https://doi.org/10.1128/AEM.65.9.3810-3819.1999	journal	September 1999
The seasonal variation of dimethyl sulfide and dimethylsulfoniopropionate concentrations in nearshore waters1: DMS/DMSP: Seasonal variation Turner, Suzanne M.; Malin, Gillian; Liss, Peter S. Limnology and Oceanography, Vol. 33, Issue 3 https://doi.org/10.4319/lo.1988.33.3.0364	journal	May 1988
Counting marine microbes with Guava Easy-Cyte 96 well plate reading flow cytometer Tripp, H. James Protocol Exchange https://doi.org/10.1038/nprot.2008.29	journal	March 2008
The riboswitch-mediated control of sulfur metabolism in bacteria Epshtein, V.; Mironov, A. S.; Nudler, E. Proceedings of the National Academy of Sciences, Vol. 100, Issue 9 https://doi.org/10.1073/pnas.0531307100	journal	April 2003
Use of Microautoradiography Combined with Fluorescence In Situ Hybridization To Determine Dimethylsulfoniopropionate Incorporation by Marine Bacterioplankton Taxa Vila, Maria; Simó, Rafel; Kiene, Ronald P. Applied and Environmental Microbiology, Vol. 70, Issue 8 https://doi.org/10.1128/AEM.70.8.4648-4657.2004	journal	August 2004
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
Release and consumption of DMSP from Emiliania huxleyi during grazing by Oxyrrhis manna Wolfe, Gv; Sherr, Eb; Sherr, Bf Marine Ecology Progress Series, Vol. 111 https://doi.org/10.3354/meps111111	journal	January 1994
Genomic islands in pathogenic and environmental microorganisms Dobrindt, Ulrich; Hochhut, Bianca; Hentschel, Ute Nature Reviews Microbiology, Vol. 2, Issue 5 https://doi.org/10.1038/nrmicro884	journal	May 2004
On the biogenic origin of dimethylsulfide: Relation between chlorophyll, ATP, organismic DMSP, phytoplankton species, and DMS distribution in Atlantic surface water and atmosphere Bürgermeister, S.; Zimmermann, R. L.; Georgii, H. -W. Journal of Geophysical Research, Vol. 95, Issue D12 https://doi.org/10.1029/JD095iD12p20607	journal	January 1990
Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes Curson, Andrew R. J.; Todd, Jonathan D.; Sullivan, Matthew J. Nature Reviews Microbiology, Vol. 9, Issue 12 https://doi.org/10.1038/nrmicro2653	journal	October 2011
Structure of the SAM-II riboswitch bound to S-adenosylmethionine Gilbert, Sunny D.; Rambo, Robert P.; Van Tyne, Daria Nature Structural & Molecular Biology, Vol. 15, Issue 2 https://doi.org/10.1038/nsmb.1371	journal	January 2008
Ecosystem-specific selection pressures revealed through comparative population genomics Coleman, M. L.; Chisholm, S. W. Proceedings of the National Academy of Sciences, Vol. 107, Issue 43 https://doi.org/10.1073/pnas.1009480107	journal	October 2010
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific Rusch, Douglas B.; Halpern, Aaron L.; Sutton, Granger PLoS Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pbio.0050077	journal	March 2007
Regulation of osmC Gene Expression by the Two-Component System rcsB-rcsC inEscherichia coli Davalos-Garcia, Marcela; Conter, Annie; Toesca, Isabelle Journal of Bacteriology, Vol. 183, Issue 20 https://doi.org/10.1128/JB.183.20.5870-5876.2001	journal	October 2001
Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria Reisch, Chris R.; Stoudemayer, Melissa J.; Varaljay, Vanessa A. Nature, Vol. 473, Issue 7346 https://doi.org/10.1038/nature10078	journal	May 2011
Dimethylsulfoniopropionate and Methanethiol Are Important Precursors of Methionine and Protein-Sulfur in Marine Bacterioplankton Kiene, Ronald P.; Linn, Laura J.; González, José Applied and Environmental Microbiology, Vol. 65, Issue 10 https://doi.org/10.1128/AEM.65.10.4549-4558.1999	journal	October 1999
Abundant and diverse bacteria involved in DMSP degradation in marine surface waters Howard, Erinn C.; Sun, Shulei; Biers, Erin J. Environmental Microbiology, Vol. 10, Issue 9 https://doi.org/10.1111/j.1462-2920.2008.01665.x	journal	September 2008
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1145	journal	November 2015
Grazing-activated chemical defence in a unicellular marine alga Wolfe, Gordon V.; Steinke, Michael; Kirst, Gunter O. Nature, Vol. 387, Issue 6636 https://doi.org/10.1038/43168	journal	June 1997
Phosphate acquisition genes in Prochlorococcus ecotypes: Evidence for genome-wide adaptation Martiny, A. C.; Coleman, M. L.; Chisholm, S. W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 33 https://doi.org/10.1073/pnas.0601301103	journal	August 2006
Turnover of Dissolved DMSP in Estuarine and Shelf Waters of the Northern Gulf of Mexico Kiene, Ronald P. Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds https://doi.org/10.1007/978-1-4613-0377-0_29	book	January 1996
Implications of streamlining theory for microbial ecology Giovannoni, Stephen J.; Cameron Thrash, J.; Temperton, Ben The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.60	journal	April 2014
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 significance of nitrogen cost minimization in proteomes of marine microorganisms Grzymski, Joseph J.; Dussaq, Alex M. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.72	journal	June 2011
Atmospheric Dimethyl Sulphide and the Natural Sulphur Cycle Lovelock, J. E.; Maggs, R. J.; Rasmussen, R. A. Nature, Vol. 237, Issue 5356 https://doi.org/10.1038/237452a0	journal	June 1972
Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean Santoro, Alyson E.; Dupont, Christopher L.; Richter, R. Alex Proceedings of the National Academy of Sciences, Vol. 112, Issue 4 https://doi.org/10.1073/pnas.1416223112	journal	January 2015
Ocean-atmosphere interactions in the global biogeochemical sulfur cycle Andreae, Meinrat O. Marine Chemistry, Vol. 30 https://doi.org/10.1016/0304-4203(90)90059-L	journal	January 1990
Transcriptional and Translational Regulatory Responses to Iron Limitation in the Globally Distributed Marine Bacterium Candidatus Pelagibacter ubique Smith, Daniel P.; Kitner, Joshua B.; Norbeck, Angela D. PLoS ONE, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pone.0010487	journal	May 2010
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
Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea Sowell, Sarah M.; Wilhelm, Larry J.; Norbeck, Angela D. The ISME Journal, Vol. 3, Issue 1 https://doi.org/10.1038/ismej.2008.83	journal	September 2008
Proteomic analyses using an accurate mass and time tag strategy Paša-Tolić, Ljiljana; Masselon, Christophe; Barry, Richard C. BioTechniques, Vol. 37, Issue 4 https://doi.org/10.2144/04374RV01	journal	October 2004
The distribution of dimethyl sulphide and dimethylsulphoniopropionate in Antarctic waters and sea ice Turner, S. M.; Nightingale, P. D.; Broadgate, W. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 42, Issue 4-5 https://doi.org/10.1016/0967-0645(95)00066-Y	journal	January 1995
Bacillus subtilis Cysteine Synthetase Is a Global Regulator of the Expression of Genes Involved in Sulfur Assimilation Albanesi, Daniela; Mansilla, Maria Cecilia; Schujman, Gustavo E. Journal of Bacteriology, Vol. 187, Issue 22 https://doi.org/10.1128/JB.187.22.7631-7638.2005	journal	November 2005
A Novel Putrescine Utilization Pathway Involves γ-Glutamylated Intermediates of Escherichia coli K-12 Kurihara, Shin; Oda, Shinpei; Kato, Kenji Journal of Biological Chemistry, Vol. 280, Issue 6 https://doi.org/10.1074/jbc.M411114200	journal	December 2004
The chemistry and biochemistry of heme c: functional bases for covalent attachment Bowman, Sarah E. J.; Bren, Kara L. Natural Product Reports, Vol. 25, Issue 6 https://doi.org/10.1039/b717196j	journal	January 2008
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Genomic island variability facilitates Prochlorococcus–virus coexistence Avrani, Sarit; Wurtzel, Omri; Sharon, Itai Nature, Vol. 474, Issue 7353 https://doi.org/10.1038/nature10172	journal	June 2011
Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC Lesniak, Jacob; Barton, William A.; Nikolov, Dimitar B. Protein Science, Vol. 12, Issue 12 https://doi.org/10.1110/ps.03375603	journal	December 2003
Algal Production of Dimethyl Sulfide and its Atmospheric Role1 Malin, Gillian; Kirst, Gunter O. Journal of Phycology, Vol. 33, Issue 6 https://doi.org/10.1111/j.0022-3646.1997.00889.x	journal	December 1997
Distribution and turnover of dissolved DMSP and its relationship with bacterial production and dimethylsulfide in the Gulf of Mexico Kiene, Ronald P.; Linn, Laura J. Limnology and Oceanography, Vol. 45, Issue 4 https://doi.org/10.4319/lo.2000.45.4.0849	journal	June 2000
Regulation of Bacterial gene Expression by Riboswitches Winkler, Wade C.; Breaker, Ronald R. Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121336	journal	October 2005
Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria Carini, Paul; White, Angelicque E.; Campbell, Emily O. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5346	journal	July 2014
Dimethylsulfoniopropionate Metabolism by Pfiesteria-Associated Roseobacter spp. Miller, T. R.; Belas, R. Applied and Environmental Microbiology, Vol. 70, Issue 6 https://doi.org/10.1128/AEM.70.6.3383-3391.2004	journal	June 2004
Comparative genomics of the methionine metabolism in Gram-positive bacteria: a variety of regulatory systems Rodionov, D. A. Nucleic Acids Research, Vol. 32, Issue 11 https://doi.org/10.1093/nar/gkh659	journal	June 2004
Identification of candidate structured RNAs in the marine organism 'Candidatus Pelagibacter ubique' Meyer, Michelle M.; Ames, Tyler D.; Smith, Daniel P. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-268	journal	January 2009
An antioxidant function for DMSP and DMS in marine algae Sunda, W.; Kieber, D. J.; Kiene, R. P. Nature, Vol. 418, Issue 6895 https://doi.org/10.1038/nature00851	journal	July 2002
Linking a Bacterial Taxon to Sulfur Cycling in the Sea: Studies of the Marine Roseobacter Group Moran, Mary Ann; González, José M.; Kiene, Ronald P. Geomicrobiology Journal, Vol. 20, Issue 4 https://doi.org/10.1080/01490450303901	journal	July 2003
Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate Charlson, Robert J.; Lovelock, James E.; Andreae, Meinrat O. Nature, Vol. 326, Issue 6114 https://doi.org/10.1038/326655a0	journal	April 1987
Conformational capture of the SAM-II riboswitch Haller, Andrea; Rieder, Ulrike; Aigner, Michaela Nature Chemical Biology, Vol. 7, Issue 6 https://doi.org/10.1038/nchembio.562	journal	May 2011
Transcriptomic Analysis of the Sulfate Starvation Response of Pseudomonas aeruginosa Tralau, Tewes; Vuilleumier, Stéphane; Thibault, Christelle Journal of Bacteriology, Vol. 189, Issue 19 https://doi.org/10.1128/JB.00889-07	journal	August 2007
Rubrerythrin and Rubredoxin Oxidoreductase inDesulfovibrio vulgaris: a Novel Oxidative Stress Protection System Lumppio, Heather L.; Shenvi, Neeta V.; Summers, Anne O. Journal of Bacteriology, Vol. 183, Issue 1 https://doi.org/10.1128/JB.183.1.101-108.2001	journal	January 2001
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
The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity Schwalbach, M. S.; Tripp, H. J.; Steindler, L. Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02092.x	journal	February 2010
Transcription termination control of the S box system: Direct measurement of S-adenosylmethionine by the leader RNA McDaniel, B. A. M.; Grundy, F. J.; Artsimovitch, I. Proceedings of the National Academy of Sciences, Vol. 100, Issue 6 https://doi.org/10.1073/pnas.0630422100	journal	March 2003

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