Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria

Genome Biology

Volumn 9, Issue 5, 2008, Pages

  Dufresne, Alexis ^a,b   Ostrowski, Martin ^c   Scanlan, David J ^c   Garczarek, Laurence ^a   Mazard, Sophie ^c   Palenik, Brian P ^d   Paulsen, Ian T ^e   de Marsac, Nicole Tandeau ^f   Wincker, Patrick ^g   Dossat, Carole ^g   Ferriera, Steve ^h   Johnson, Justin ^h   Post, Anton F ⁱ   Hess, Wolfgang R ^j   Partensky, Frédéric ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MACQUARIE UNIVERSITY   (Australia)

^f CNRS   (France)

^g UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^h J CRAIG VENTER INSTITUTE   (United States)

ⁱ The Interuniversity Institute for Marine Science Eilat   (Israel)

^j UNIVERSITY OF FREIBURG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM ISOLATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYANOBACTERIUM; ECOLOGICAL NICHE; EVOLUTIONARY HOMOLOGY; GENE FUNCTION; GENE NUMBER; GENE TRANSFER; GENETIC LINE; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; GENOMIC ISLAND; GEOGRAPHIC DISTRIBUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPECIES COMPARISON; STRAIN IDENTIFICATION; SYNECHOCOCCUS; BACTERIAL GENOME; CLASSIFICATION; GENETICS; HORIZONTAL GENE TRANSFER; MICROBIOLOGY;

CYANOBACTERIA; SYNECHOCOCCUS;

SEA WATER;

GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; SEAWATER; SYNECHOCOCCUS;

EID: 47149092637     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2008-9-5-r90     Document Type: Article

References (63)

1. Goericke R Welschmeyer NA The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res 1993, 40:2283-2294 10.1016/ 0967-0637(93)90104-B
2. Li WKW Primary productivity of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting. Limnol Oceanogr 1994, 39:169-175
3. Moran XAG Fernandez E Perez V Size-fractionated primary production, bacterial production and net community production in subtropical and tropical domains of the oligotrophic NE Atlantic in autumn. Mar Ecol Prog Ser 2004, 274:17-29 10.3354/meps274017
4. Scanlan DJ West NJ Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 2002, 40:1-12 10.1111/j.1574-6941.2002.tb00930.x
5. Olson RJ Zettler ER Armbrust EV Chisholm SW Pigment, size and distribution of Synechococcus in the North Atlantic and Pacific oceans. Limnol Oceanogr 1990, 35:45-58
6. Partensky F Blanchot J Vaulot D Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: A review. Marine Cyanobacteria Monaco: Musée Océanographique Charpy L, Larkum A 1999, 19:457-475
7. Olson RJ Zettler ER Altabet MA Dusenberry JA Chisholm SW Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep-Sea Res 1990, 37:1033-1051 10.1016/ 0198-0149(90)90109-9
8. Partensky F Hess WR Vaulot D Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 1999, 63:106-127 98958 10066832
9. Tarran GA Zubkov MV Sleigh MA Burkill PH Yallop M Microbial community structure and standing stocks in the NE Atlantic in June and July of 1996. Deep-Sea Res II 2001, 48:963-985 10.1016/S0967-0645(00)00104-1
10. Moore LR Rocap G Chisholm SW Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 1998, 393:464-467 10.1038/ 30965 9624000
11. Johnson ZI Zinser ER Coe A McNulty NP Woodward EM Chisholm SW Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 2006, 311:1737-1740 10.1126/ science.1118052 16556835
12. Fuller NJ Marie D Partensky F Vaulot D Post AF Scanlan DJ Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 2003, 69:2430-2443 154553 12732508 10.1128/AEM.69.5.2430-2443.2003
13. Ahlgren NA Rocap G Culture isolation and culture-independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. Appl Environ Microbiol 2006, 72:7193-7204 1636174 16936060 10.1128/AEM.00358-06
14. Muhling M Fuller NJ Somerfield PJ Post AF Wilson WH Scanlan DJ Joint I Mann NH High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length polymorphism. Aquat Microb Ecol 2006, 45:263-275 10.3354/ame045263
15. Penno S Lindell D Post AF Diversity of Synechococcus and Prochlorococcus populations determined from DNA sequences of the N-regulatory gene ntcA. Environ Microbiol 2006, 8:1200-1211 10.1111/j.1462-2920.2006.01010.x 16817928
16. Toledo G Palenik B Brahamsha B Swimming marine Synechococcus strains with widely different photosynthetic pigment ratios form a monophyletic group. Appl Environ Microbiol 1999, 65:5247-5251 91712 10583972
17. Ferris MJ Palenik B Niche adaptation in ocean cyanobacteria. Nature 1998, 396:226-228 10.1038/24297
18. Fuller NJ Tarran GA Yallop M Orcutt KM Scanlan DJ Molecular analysis of picocyanobacterial community structure along an Arabian Sea transect reveals distinct spatial separation of lineages. Limnol Oceanogr 2006, 51:2515-2526
19. Zwirglmaier K Heywood JL Chamberlain K Woodward EMS Zubkov MV Scanlan DJ Basin-scale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ Microbiol 2007, 9:1278-1290 10.1111/ j.1462-2920.2007.01246.x 17472640
20. Toledo G Palenik B A Synechococcus serotype is found preferentially in surface marine waters. Limnol Oceanogr 2003, 48:1744-1755
21. Zwirglmaier K Jardillier L Ostrowski M Mazard S Garczarek L Vaulot D Not F Massana R Ulloa O Scanlan DJ Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 2008, 10:147-161 17900271
22. Rocap G Larimer FW Lamerdin J Malfatti S Chain P Ahlgren NA Arellano A Coleman M Hauser L Hess WR Johnson ZI Land M Lindell D Post AF Regala W Shah M Shaw SL Steglich C Sullivan MB Ting CS Tolonen A Webb EA Zinser ER Chisholm SW Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 2003, 424:1042-1047 10.1038/nature01947 12917642
23. Kettler G Martiny AC Huang K Zucker J Coleman ML Rodrigue S Chen F Lapidus A Ferriera S Johnson J Steglich C Church G Richardson P Chisholm SW Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 2007, 3:e231 2151091 18159947 10.1371/ journal.pgen.0030231
24. Dufresne A Garczarek L Partensky F Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 2005, 6:R14 551534 15693943 10.1186/gb-2005-6-2-r14
25. Coleman ML Sullivan MB Martiny AC Steglich C Barry K Delong EF Chisholm SW Genomic islands and the ecology and evolution of Prochlorococcus. Science 2006, 311:1768-1770 10.1126/science.1122050 16556843
26. Palenik B Brahamsha B Larimer FW Land M Hauser L Chain P Lamerdin J Regala W Allen EE McCarren J Paulsen I Dufresne A Partensky F Webb EA Waterbury J The genome of a motile marine Synechococcus. Nature 2003, 424:1037-1042 10.1038/nature01943 12917641
27. Palenik B Ren QH Dupont CL Myers GS Heidelberg JF Badger JH Madupu R Nelson WC Brinkac LM Dodson RJ Durkin AS Daugherty SC Sullivan SA Khouri H Mohamoud Y Halpin R Paulsen IT Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 2006, 103:13555-13559 1569201 16938853 10.1073/ pnas.0602963103
28. Mulkidjanian AY Koonin EV Makarova KS Mekhedov SL Sorokin A Wolf YI Dufresne A Partensky F Burd H Kaznadzey D Haselkorn R Galperin MY The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 2006, 103:13126-13131 1551899 16924101 10.1073/ pnas.0605709103
29. Six C Thomas J-C Garczarek L Ostrowski M Dufresne A Blot N Scanlan DJ Partensky F Diversity and evolution of phycobilisomes in marine Synechococcus spp. - a comparative genomics study. Genome Biol 2007, 8:R259 2246261 18062815 10.1186/gb-2007-8-12-r259
30. Hess WR Rocap G Ting CS Larimer F Stilwagen S Lamerdin J Chisholm SW The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics. Photosynth Res 2001, 70:53-71 10.1023/ A:1013835924610 16228362
31. Steglich C Frankenberg-Dinkel N Penno S Hess WR A green light-absorbing phycoerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp. MED4. Environ Microbiol 2005, 7:1611-1618 10.1111/ j.1462-2920.2005.00855.x 16156734
32. Badger MR Price GD CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 2003, 54:609-622 10.1093/jxb/erg076 12554704
33. Schürmann P Jacquot JP Plant thioredoxin systems revisited. Ann Rev Plant Physiol Plant Mol Biol 2000, 51:371-400 10.1146/ annurev.arplant.51.1.371
34. Geiss U Vinnemeier J Kunert A Lindner I Gemmer B Lorenz M Hagemann M Schoor A Detection of the isiA gene across cyanobacterial strains: Potential for probing iron deficiency. Appl Environ Microbiol 2001, 67:5247-5253 93297 11679352 10.1128/AEM.67.11.5247-5253.2001
35. Zurbriggen MD Tognetti VB Carrillo N Stress-inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome. Iubmb Life 2007, 59:355-360 10.1080/15216540701258744 17505975
36. Erdner DL Price NM Doucette GJ Peleato ML Anderson DM Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Mar Ecol Progr Ser 1999, 184:43-53 10.3354/meps184043
37. Global Ocean Sampling (GOS) Web Site http://www.jcvi.org/cms/research/ projects/gos
38. McCarren J Brahamsha B SwmB, a 1.12-megadalton protein that is required for nonflagellar swimming motility in Synechococcus. J Bacteriol 2007, 189:1158-1162 1797281 17158680 10.1128/JB.01500-06
39. Clokie MR Millard AD Wilson WH Mann NH Encapsidation of host DNA by bacteriophages infecting marine Synechococcus strains. FEMS Microbiol Ecol 2003, 46:349-352 10.1016/S0168-6496(03)00247-2
40. Herdman M Castenholz RW Waterbury JB Rippka R Form-genus XIII. Synechococcus. Bergey's Manual of Systematic Bacteriology New York: Springer-Verlag Boone DR, Castenholz RW 2 2001, 1:508-512
41. Urbach E Scanlan DJ Distel DL Waterbury JB Chisholm SW Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 1998, 46:188-201 10.1007/ PL00006294 9452521
42. Lento GM Hickson RE Chambers GK Penny D Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 1995, 12:28-52 7877495
43. Zhaxybayeva O Lapierre P Gogarten JP Genome mosaicism and organismal lineages. Trends Genet 2004, 20:254-260 10.1016/j.tig.2004.03.009 15109780
44. Konstantinidis KT Tiedje JM Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005, 102:2567-2572 549018 15701695 10.1073/pnas.0409727102
45. Wayne LG Brenner DJ Colwell RR Grimont PAD Kandler O Krichevsky MI Moore LH Murray RGE Stackebrandt E Starr MP Trüper HG Report of the ad hoc commitee on reconciliation of approaches to bacterial systematics. Intl J Syst Bacteriol 1987, 37:463-475
46. Cohan FM Perry EB A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 2007, 17:R373-386 10.1016/ j.cub.2007.03.032 17502094
47. Haverkamp T Acinas SG Doeleman M Stomp M Huisman J Stal LJ Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons. Environ Microbiol 2008, 10:174-188 17903216 17903216
48. Dufresne A Salanoubat M Partensky F Artiguenave F Axmann IM Barbe V Duprat S Galperin MY Koonin EV Le Gall F Makarova KS Ostrowski M Oztas S Robert C Rogozin IB Scanlan DJ Tandeau de Marsac N Weissenbach J Wincker P Wolf YI Hess WR Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 2003, 100:10020-10025 187748 12917486 10.1073/pnas.1733211100
49. Bibby TS Nield J Chen M Larkum AW Barber J Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system. Proc Natl Acad Sci USA 2003, 100:9050-9054 166436 12837938 10.1073/pnas.1532271100
50. Garczarek L Dufresne A Rousvoal S West NJ Mazard S Marie D Claustre H Raimbault P Post AF Scanlan DJ Partensky F High vertical and low horizontal diversity of Prochlorococcus ecotypes in the Mediterranean Sea in summer. FEMS Microbiol Ecol 2007, 60:189-206 10.1111/ j.1574-6941.2007.00297.x 17391326
51. Rocap G Distel DL Waterbury JB Chisholm SW Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 2002, 68:1180-1191 123739 11872466 10.1128/AEM.68.3.1180-1191.2002
52. Altschul SF Madden TL Schaffer AA Zhang J Zhang Z Miller W Lipman DJ Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402 146917 9254694 10.1093/ nar/25.17.3389
53. Enright AJ van Dongen S Ouzounis CA An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584 101833 11917018 10.1093/nar/30.7.1575
54. Cyanorak Database http://www.sb-roscoff.fr/Phyto/cyanorak
55. Hsiao WWL Ung K Aeschliman D Bryan J Finlay BB Brinkman FSL Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet 2005, 1:e62 1285063 16299586 10.1371/journal.pgen.0010062
56. Rusch DB Halpern AL Sutton G Heidelberg KB Williamson S Yooseph S Wu D Eisen JA Hoffman JM Remington K Beeson K Tran B Smith H Baden-Tillson H Stewart C Thorpe J Freeman J Andrews-Pfannkoch C Venter JE Li K Kravitz S Heidelberg JF Utterback T Rogers Y-H Falcon LI Souza V Bonilla-Rosso G Eguiarte LE Karl DM Sathyendranath S The Sorcerer II global ocean sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol 2007, 5:e77 1821060 17355176 10.1371/ journal.pbio.0050077
57. Phrap, Phred, Consed Web Site http://www.phrap.org/phredphrapconsed.html
58. Edgar RC MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797 390337 15034147 10.1093/ nar/gkh340
59. Castresana J Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552 10742046
60. Schmidt HA Strimmer K Vingron M von Haeseler A TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18:502-504 10.1093/bioinformatics/18.3.502 11934758
61. Felsenstein J PHYLIP - Phylogeny inference package (version 3.2). Cladistics 1989, 5:164-166
62. Guindon S Gascuel O A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704 10.1080/10635150390235520 14530136
63. Huson DH Steel M Phylogenetic trees based on gene content. Bioinformatics 2004, 20:2044-2049 10.1093/bioinformatics/bth198 15044248