Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Newton, Irene L G ^a,b   Girguis, Peter R ^a   Cavanaugh, Colleen M ^a  

^a HARVARD UNIVERSITY   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; CHEMOAUTOTROPHY; CLAM; COLD SEEP SPECIES; COMPARATIVE GENOMIC HYBRIDIZATION; DNA CONTENT; EUKARYOTE EVOLUTION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CONSERVATION; HETEROLOGOUS EXPRESSION; HYDROTHERMAL VENT SPECIES; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIONT; ANIMAL; BACTERIAL GENOME; BIOLOGY; BIVALVE; COMPARATIVE STUDY; DNA MICROARRAY; DNA SEQUENCE; GAMMAPROTEOBACTERIA; GENETICS; GENOMICS; MICROBIOLOGY; MOLECULAR EVOLUTION; SYMBIOSIS;

BIVALVIA; GAMMAPROTEOBACTERIA; INVERTEBRATA; MOLLUSCA; VESICOMYIDAE;

BACTERIAL DNA;

ANIMALS; BIVALVIA; COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GAMMAPROTEOBACTERIA; GENOME, BACTERIAL; GENOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 60549115337     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-585     Document Type: Article

References (63)

1. Bonfante P Plants, mycorrhizal fungi and endobacteria: A dialog among cells and genomes Biol Bull 2003, 204(2):215-220. 10.2307/1543562 12700157
2. Buchner P Endosymbiosis of animals with plant microorganisms New York: interscience Publishers, Inc 1965.
3. Margulis L Fester R Symbiosis as a source of evolutionary innovation Cambridge, MA: MIT Press 1991.
4. Stewart FJ Newton IL Cavanaugh CM Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces Trends Microbiol 2005, 13(9):439-448. 10.1016/j.tim.2005.07.007 16054816
5. Cavanaugh CM McKiness ZP Newton ILG Stewart F Marine Chemosynthetic Symbioses The Prokaryotes Berlin: Springer-Verlag 2004.
6. Cavanaugh CM Microbial symbiosis: Patterns of diversity in the marine environment Amer Zool 1994, 34:79-89.
7. Distel D Evolution of chemoautotrophic endosymbioses in bivalves BioScience 1998, 48:277-286. 10.2307/1313354
8. Nelson D Fisher C Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps Microbiology of deep-sea hydrothermal vents Boca Raton: CRC Press Karl D 1995.
9. Kiel S Little CT Cold-seep mollusks are older than the general marine mollusk fauna Science 2006, 313(5792):1429-1431. 10.1126/science.1126286 16960004
10. Boss KJ Turner RD The giant white clam from the Galapagos Rift, Calyptogena magnifica species novum Malacologia 1980, 20(1):161-194.
11. Childress JJ Fisher CR Favuzzi JA Sanders NK Sulfide and carbon dioxide uptake by the hydrothermal vent clam, Calyptogena magnifica and its chemoautotrophic symbionts Physiol Zool 1991, 64:1444-1470.
12. Robinson JJ Cavanaugh CM Expressions of form I and form II Rubisco in chemoautotrophic symbioses: Implications for the interpretation of stable carbon isotope values Limnol Oceanogr 1995, 40:1496-1502.
13. 2 fixation in chemoautotroph-invertebrate symbioses: Expression of Form I and Form II RuBisCO Microbial Growth on C1 Compounds Dordrecht, The Netherlands: Kluwer Academic Publishers Lidstrom ME, Tabita FR 1996:285-292.
14. Peek AS Feldman RA Lutz RA Vrijenhoek RC Cospeciation of chemoautotrophic bacteria and deep sea clams Proceedings of the National Academy of Science 1998, 95:9962-9966. 10.1073/pnas.95.17.9962
15. Cary SC Giovannoni SJ Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps Proceedings Of The National Academy Of Sciences Of The United States Of America 1993, 90(12):5695-5699. 46788 8100068 10.1073/pnas.90.12.5695
16. Endow K Ohta S Occurrence of bacteria in the primary oocytes of the vesicomyid clam Calyptogena soyoae Mar Ecol Prog Ser 1990, 64:309-311. 10.3354/meps064309
17. Wernegreen JJ Endosymbiosis: Lessons in conflict resolution PLoS Biol 2004, 2(3):E68. 368163 15024418 10.1371/journal.pbio.0020068
18. Akman L Yamashita A Watanabe H Oshima K Shiba T Hattori M Aksoy S Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia Nat Genet 2002, 32(3):402-407. 10.1038/ng986 12219091
19. Wernegreen JJ Lazarus AB Degnan PH Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle Microbiology 2002, 148(Pt 8):2551-2556. 12177348
20. van Ham RC Kamerbeek J Palacios C Rausell C Abascal F Bastolla U Fernandez JM Jimenez L Postigo M Silva FJ et al. Reductive genome evolution in Buchnera aphidicola Proc Natl Acad Sci USA 2003, 100(2):581-586. 141039 12522265 10.1073/pnas.0235981100
21. Wu D Daugherty SC Aken SE Pai GH Watkins KL Khouri H Tallon LJ Zaborsky JM Dunbar HE Tran PL et al Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters PLoS Biol 2006, 4(6):e188. 1472245 16729848 10.1371/journal.pbio.0040188
22. Tamas I Klasson L Canback B Naslund AK Eriksson AS Wernegreen JJ Sandstrom JP Moran NA Andersson SG 50 million years of genomic stasis in endosymbiotic bacteria Science 2002, 296(5577):2376-2379. 10.1126/ science.1071278 12089438
23. Canback B Tamas I Andersson SG A phylogenomic study of endosymbiotic bacteria Mol Biol Evol 2004, 21(6):1110-1122. 10.1093/molbev/msh122 15014155
24. Latorre A Gil R Silva FJ Moya A Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola Heredity 2005, 95(5):339-347. 10.1038/sj.hdy.6800716 16118664
25. Degnan PH Lazarus AB Wernegreen JJ Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects Genome Res 2005, 15(8):1023-1033. 1182215 16077009 10.1101/gr.3771305
26. Zientz E Dandekar T Gross R Metabolic interdependence of obligate intracellular bacteria and their insect hosts Microbiol Mol Biol Rev 2004, 68(4):745-770. 539007 15590782 10.1128/MMBR.68.4.745-770.2004
27. McGraw EA O'Neill SL Evolution of Wolbachia pipientis transmission dynamics in insects Trends Microbiol 1999, 7(7):297-302. 10.1016/ S0966-842X(99)01531-0 10390640
28. Noda H Miyoshi T Zhang Q Watanabe K Deng K Hoshizaki S Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparAsite (Strepsiptera: Elenchidae): a probable case of interspecies transmission Mol Ecol 2001, 10(8):2101-2106. 10.1046/ j.0962-1083.2001.01334.x 11555254
29. Fenn K Blaxter M Wolbachia genomes: Revealing the biology of parasitism and mutualism Trends in Parasitology 2005, 22:60-65. 10.1016/ j.pt.2005.12.012
30. Wu M Sun LV Vamathevan J Riegler M Deboy R Brownlie JC McGraw EA Martin W Esser C Ahmadinejad N et al Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements PLoS Biol 2004, 2(3):E69. 368164 15024419 10.1371/ journal.pbio.0020069
31. Stewart FJ Young CR Cavanaugh CM Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis Mol Biol Evol 2008, 25(4):673-687. 10.1093/molbev/msn010 18192696
32. Stewart FJ Genetic diversification and evolution of chemosynthetic endosymbionts in deep-sea clams (Vesicomyidae) Cambridge: Harvard University 2008.
33. Newton IL Woyke T Auchtung TA Dilly GF Dutton RJ Fisher MC Fontanez KM Lau E Stewart FJ Richardson PM et al The Calyptogena magnifica chemoautotrophic symbiont genome Science 2007, 315:5814-998. 1000 10.1126/science.1138438 17303757
34. Kuwahara H Yoshida T Takaki Y Shimamura S Nishi S Harada M Matsuyama K Takishita K Kawato M Uematsu K et al Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii Curr Biol 2007, 17(10):881-886. 10.1016/j.cub.2007.04.039 17493812
35. McGraw E O'Neill S Evolution of Wolbachia pipientis transmission dynamics in insects Trends Microbiol 1999, 7:297-302. 10.1016/ S0966-842X(99)01531-0 10390640
36. Moran NA Tracing the evolution of gene loss in obligate bacterial symbionts Curr Opin Microbiol 2003, 6(5):512-518. 10.1016/ j.mib.2003.08.001 14572545
37. Jannasch HW Wirsen CO Nelson DC Robertson LA et al Thiomicrospira crunogena sp. nov., a colorless sulfur-oxidizing bacterium from a deep-sea hydrothermal vent Int J Syst Bacteriol 1985, 35:422-424.
38. Scott KM Sievert SM Abril FN Ball LA Barrett CJ Blake RA Boller AJ Chain PS Clark JA Davis CR et al. The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2 PLoS Biol 2006, 4(12):e383. 1635747 17105352 10.1371/journal.pbio.0040383
39. Kuwahara H Takaki Y Yoshida T Shimamura S Takishita K Reimer JD Kato C Maruyama T Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams Extremophiles 2008, 12(3):365-374. 10.1007/s00792-008-0141-2 18305898
40. Goffredi SK Hurtado LA Hallam S Vrijenhoek RC Evolutionary relationships of deep-sea vent and cold seep clams (Mollusca: Vesicomyidae) of the "pacifica/lepta" species complex Marine Biology 2003, 142(2):311-320.
41. Kato-Maeda M Rhee JT Gingeras TR Salamon H Drenkow J Smittipat N Small PM Comparing genomes within the species Mycobacterium tuberculosis Genome Res 2001, 11(4):547-554. 311074 11282970 10.1101/gr.166401
42. Marokhazi J Waterfield N LeGoff G Feil E Stabler R Hinds J Fodor A ffrench-Constant RH Using a DNA microarray to investigate the distribution of insect virulence factors in strains of photorhabdus bacteria J Bacteriol 2003, 185(15):4648-4656. 165762 12867479 10.1128/ JB.185.15.4648-4656.2003
43. Wolfgang MC Kulasekara BR Liang X Boyd D Wu K Yang Q Miyada CG Lory S Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa Proc Natl Acad Sci USA 2003, 100(14):8484-8489. 166255 12815109 10.1073/pnas.0832438100
44. Cassat JE Dunman PM McAleese F Murphy E Projan SJ Smeltzer MS Comparative genomics of Staphylococcus aureus musculoskeletal isolates J Bacteriol 2005, 187(2):576-592. 543526 15629929 10.1128/ JB.187.2.576-592.2005
45. Stolz JF Basu P Evolution of nitrate reductase: Molecular and structural variations on a common function Chembiochem 2002, 3(2-3):198-206. 10.1002/1439-7633(20020301)3:2/3<198::AID-CBIC198>3.0.CO;2-C 11921398
46. Wood AP Aurikko JP Kelly DP A challenge for 21st century molecular biology and biochemistry: What are the causes of obligate autotrophy and methanotrophy? Fems Microbiology Reviews 2004, 28(3):335-352. 10.1016/ j.femsre.2003.12.001 15449607
47. Shively JM van Keulen G Meijer WG Something from almost nothing: Carbon dioxide fixation in chemoautotrophs Annu Rev Microbiol 1998, 52:191-230. 10.1146/annurev.micro.52.1.191 9891798
48. Cannon GC Bradburne CE Aldrich HC Baker SH Heinhorst S Shively JM Microcompartments in prokaryotes: Carboxysomes and related polyhedra Appl Environ Microbiol 2001, 67(12):5351-5361. 93316 11722879 10.1128/ AEM.67.12.5351-5361.2001
49. Scott KM A delta13C-based carbon flux model for the hydrothermal vent chemoautotrophic symbiosis Riftia pachyptila predicts sizeable CO(2) gradients at the host-symbiont interface Environ Microbiol 2003, 5(5):424-432. 10.1046/j.1462-2920.2003.00416.x 12713468
50. Pires RH Venceslau SS Morais F Teixeira M Xavier AV Pereira IA Characterization of Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex - a membrane-bound redox complex involved in the sulfate respiratory pathway Biochemistry 2006, 45(1):249-262. 10.1021/bi0515265 16388601
51. Dahl C Engels S Pott-Sperling AS Schulte A Sander J Lubbe Y Deuster O Brune DC Novelgenes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum J Bacteriol 2005, 187(4):1392-1404. 545617 15687204 10.1128/JB.187.4.1392-1404.2005
52. Blasco F Iobbi C Giordano G Chippaux M Bonnefoy V Nitrate reductase of Escherichia coli: Completion of the nucleotide sequence of the nar operon and reassessment of the role of the alpha and beta subunits in iron binding and electron transfer Mol Gen Genet 1989, 218(2):249-256. 10.1007/BF00331275 2674654
53. Jormakka M Richardson D Byrne B Iwata S Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes Structure 2004, 12(1):95-104. 10.1016/j.str.2003.11.020 14725769
54. Johnson KS Childress JJ Hessler RR Sakamoto-Arnold CM Beehler CL Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center Deep-Sea Research 1988, 35:1723-1744. 10.1016/0198-0149(88)90046-5
55. Masuzawa T Handa N Kitagawa H Kusakabe M Sulfate reduction using methane in sediments beneath a bathyal "cold seep" giant clam community off Hatsushima Island, Sagami Bay, Japan Earth and Planetary Science Letters 1992, 110:39-50. 10.1016/0012-821X(92)90037-V
56. Terwilliger RC Terwilliger NB Arp A Thermal vent clam (Calyptogena-Magnifica) hemoglobin Science 1983, 219(4587):981-983. 10.1126/science.219.4587.981 17817936
57. Kawano K Iwasaki N Suzuki T Notable diversity in hemoglobin expression patterns among species of the deep-sea clam, Calyptogena Cell Mol Life Sci 2003, 60(9):1952-1956. 10.1007/s00018-003-3184-7 14523555
58. Fath MJ Kolter R ABC transporters: Bacterial exporters Microbiol Rev 1993, 57(4):995-1017. 372944 8302219
59. Fialamedioni A Michalski JC Jolles J Alonso C Montreuil J Lysosomic and lysozyme activities in the gill of bivalves from deep hydrothermal vents Comptes Rendus Acad Sci Ser III-Sci Vie-Life Sci 1994, 317(3):239-244.
60. Conway NM Occurrence of lysozyme in the common cockle Cerastoderma edule and the effect of the tidal cycle on lysozyme activity Marine Biology 1987, 95:231-235. 10.1007/BF00409010
61. Wall DP Fraser HB Hirsh AE Detecting putative orthologs Bioinformatics 2003, 19(13):1710-1711. 10.1093/bioinformatics/btg213 15593400
62. Kurtz S Phillippy A Delcher AL Smoot M Shumway M Antonescu C Salzberg SL Versatile and open software for comparing large genomes Genome Biol 2004, 5(2):R12. 395750 14759262 10.1186/gb-2004-5-2-r12
63. Altschul SF Gish W Miller W Myers EW Lipman DJ Basic local alignment search tool J Mol: Biol 1990, 215(3):403-410. 2231712