Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea osedax worms

ISME Journal

Volumn 8, Issue 4, 2014, Pages 908-924

  Goffredi, Shana K ^a,e   Yi, Hana ^b,e   Zhang, Qingpeng ^c   Klann, Jane E ^a   Struve, Isabelle A ^a   Vrijenhoek, Robert C ^d   Brown, C Titus ^c  

^a OCCIDENTAL COLLEGE   (United States)

^b Seoul National University   (South Korea)

^c Michigan State University   (United States)

^d MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

^e Korea University   (South Korea)

Author keywords

Deep sea; Oceanospirillales; Osedax; Symbionts; Whale fall

Indexed keywords

DEEP-SEA BENTHOS; FUNCTIONAL CHANGE; GENOMICS; HETEROTROPHY; POLYCHAETE; SYMBIONT; WHALE;

MONTEREY CANYON; PACIFIC OCEAN;

CETACEA; OCEANOSPIRILLALES; OSEDAX; POLYCHAETA;

CARBON; RNA 16S;

ADAPTATION; ANIMAL; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CLASSIFICATION; FEMALE; GAMMAPROTEOBACTERIA; GENETIC VARIABILITY; GENETICS; HETEROTROPHY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; POLYCHAETA; SYMBIOSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CARBON RADIOISOTOPES; FEMALE; GAMMAPROTEOBACTERIA; GENES, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; HETEROTROPHIC PROCESSES; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYCHAETA; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84899438331     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.201     Document Type: Article

References (101)

1. Actis LA, Fish W, Crosa JH, Kellerman K, Ellenberger SR, Hauser FM et al. (1986). Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775(pJM1). J Bacteriol 167: 57-65.
2. Arahal DR, Lekunberri I, González JM, Pascual J, Pujalte MJ, PedroPedrós-AlióC et al. (2007). Neptuniibacter caesariensis gen. nov., sp. nov., a novel marine genome-sequenced gammaproteobacterium. Int J Syst Evol Microbiol 57: 1000-1006.
3. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al. (2008). The RAST Server: Rapid annotations using subsystems technology. BMC Genomics 9: 75.
4. Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC. (2007). Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Res Part I Oceanogr Res 54: 1773-1791.
5. Bright M, Bulgheresi S. (2010). A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218-230.
6. Brown CT, Howe A, Zhang Q, Pyrkosz AB, Brom TH. (2012). A reference-free algorithm for computational normalization of shotgun sequencing data. Genomics arXiv:12034802 (q-bioGN).
7. Chiavelli DA, Marsh JW, Taylor RK. (2001). The mannosesensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67: 3220-3225.
8. Chun J, Grim CJ, Hasan NR, Lee J, Choi SY, Haley BJ et al. (2009). Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci USA 106: 15442-15447.
9. Chun J, Kim KY, Lee JH, Choi Y. (2010). The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 10: 101.
10. Coplen TB, Brand WA, Gehre M, Gröning M, Meijer HA, Toman B et al. (2006). New guidelines for d13C measurements. Anal Chem 78: 2439-2441.
11. Craig L, Li J. (2008). Type IV pili: paradoxes in form and function. Curr Opin Struct Biol 18: 267-277.
12. Dalisay DS, Webb JS, Scheffel A, Svenson C, James S, Holmstrom C et al. (2006). A mannose-sensitive haemagglutinin (MSHA)-like pilus promotes attachment of Pseudoalteromonas tunicata cells to the surface of the green alga Ulva australis. Microbiology 152: 2875-2883.
13. Delcher AL, Bratke KA, Powers EC, Salzberg SL. (2007). Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
14. Disz T, Akhter S, Cuevas D, Olson R, Overbeek R. (2010). Accessing the SEED genome databases via Web services API: tools for programmers. BMC Bioinformatics 11: 319.
15. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, Taourit S et al. (2003). The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21: 1307-1313.
16. Dupont CL, Rusch DB, Yooseph S, Lombardo MJ, Richter RA, Valas R et al. (2012). Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J 6: 1186-1199.
17. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ. (2002). Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci USA 99: 1556-1561.
18. EisenreichW, Dandekar T, Heesemann J, GoebelW. (2010). Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8: 401-412.
19. Fang FC, Libby SJ, Castor ME, Fung AM. (2005). Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infect Immun 73: 2547-2549.
20. Felsenstein J. (1985). Confidence-limits on phylogenies- An approach using the bootstrap. Evolution 39: 783-791.
21. Ffrench-Constant RH, Waterfield N, Burland V, Perna NT, Daborn PJ, Bowen D et al. (2000). A genomic sample sequence of the entomopathogenic bacterium Photorhabdus luminescens W14: Potential implications for virulence. Appl Environ Microbiol 66: 3310-3329.
22. Finn RD, Clements J, Eddy SR. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Res Web Server Issue 39: W29-W37.
23. Fullner KJ, Boucher JC, Hanes MA, Haines GK III, Meehan BM, Walchle C et al. (2002). The contribution of accessory toxins of Vibrio cholerae O1 El tor to the proinflammatory response in a murine pulmonary cholera model. J Exp Med 195: 1455-1462.
24. Fujikura K, Fujiwara Y, Kawato M. (2006). A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zoolog Sci 23: 733-740.
25. Gaillard J-L, Berche P, Frehel C, Gouin E, Cossart P. (1991). Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65: 1127-1141.
26. Glover AG, Källström B, Smith CR, Dahlgren TG. (2005). World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc Biol Sci 272: 2587-2592.
27. Goffredi SK, Paull CK, Fulton-Bennett K, Hurtado LA, Vrijenhoek RC. (2004). Unusual benthic fauna associated with a whale-fall in Monterey Canyon, California. Deep Sea Res Part I Oceanogr Res 51: 1295-1306.
28. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K et al. (2005). Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7: 1369-1378.
29. Goffredi SK, Johnson SB, Vrijenhoek RC. (2007). Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 73: 2314-2323.
30. Goffredi SK, Wilpiszeski R, Lee R, Orphan VJ. (2008). Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California. ISME J 2: 204-220.
31. Goffredi SK, Orphan VJ. (2010). Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ Microbiol 12: 344-363.
32. Goffredi SK, Morella N, Pulcrano M. (2012). Affiliations between bacteria and marine fish leeches (Piscicolidae), with emphasis on a new deep-sea species from Monterey Canyon, CA. Environ Microbiol 14: 2429-2444.
33. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. (2007). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81-91.
34. Gould TA, van de Langemheen H, Muñoz-El?'as EJ, McKinney JD, Sacchettini JC. (2006). Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol Microbiol 61: 940-947.
35. Griffiths GL, Sigel SP, Payne SM, Neilands JB. (1984). Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259: 383-385.
36. Higgs ND, Glover AG, Dahlgren TG, Little CT. (2011). Bone-boring worms: characterizing the morphology, rate, and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae). Biol Bull 221: 307-316.
37. Higgs ND, Little CTS, Glover AG, Dahlgren TG, Smith CR. (2012). Evidence of Osedax worm borings in Pliocene (B3Ma) whale bone from the Mediterranean. Hist Biol 24: 269-277.
38. Hilário A, Capa M, Dahlgren TG, Halanych KM, Little CT, Thornhill DJ et al. (2011). New perspectives on the ecology and evolution of siboglinid tubeworms. PLoS One 6: e16309.
39. Hornung JM, Jones HA, Perry RD. (1996). The hmu locus of Yersinia pestis is essential for utilization of free haemin and haem-protein complexes as iron sources. Mol Microbiol 20: 725-739.
40. Jeong H, Yim JH, Lee C, Choi SH, Park YK, Yoon SH et al. (2005). Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res 33: 7066-7073.
41. Jukes TH, Cantor CR. (1969). Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press: New York, pp 21-132.
42. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. (2010). KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38: D355-D360.
43. Kessler JD, Valentine DL, Redmond MC, Du MR, Chan EW, Mendes SD. (2011). A persistent oxygen anomaly reveals the fate of spilled methane in the deep Gulf of Mexico. Science 331: 312-315.
44. Kiel S, Kahl W-A, Goedert JL. (2011). Osedax borings in fossil marine bird bones. Naturwissenschaften 98: 51-55.
45. Konstantinidis KT, Tiedje JM. (2004). Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci USA 101: 3160-3165.
46. Konstantinidis KT, Tiedje JM. (2005). Towards a genomebased taxonomy for prokaryotes. J Bacteriol 187: 6258-6264.
47. Koppisch AT, Browder CC, Moe AL, Shelley JT, Kinkel BA, Hersman LE et al. (2005). Petrobactin is the primary siderophore synthesized by Bacillus anthracis str Sterne under conditions of iron starvation. BioMetals 18: 577-585.
48. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D et al. (2009). Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
49. Kuhn M, Kathariou S, Goebel W. (1988). Hemolysin supports survival but not entry of the intracellular bacterium Listeria monocytogenes. Infect Immun 56: 79-82.
50. Kumar S, Nei M, Dudley J, Tamura K. (2008). MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.
51. Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M et al. (2007). Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol 17: 881-886.
52. Lauro FM, Bartlett DH. (2008). Prokaryotic lifestyles in deep sea habitats. Extremophiles 12: 15-25.
53. Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P. (1997). Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65: 5309-5319.
54. Lee JH, Yi H, Chun J. (2011). rRNASelector: a computer program for selecting ribosomal RNA encoding sequences from metagenomic and metatranscriptomic shotgun libraries. J Microbiol 49: 689-691.
55. Litwin CM, Calderwood SB. (1993). Role of iron in regulation of virulence genes. Clin Microbiol Rev 6: 137-149.
56. Ludwig W, Strunk R, Westram L, Richter H, Meier H. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
57. Lundsten L, Fraisier K, Schlining KL, Johnson SB, Kuhnz LA, Harvey JB et al. (2010). Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA. Deep Sea Res Part 1 Oceanogr Res 57: 1573-1584.
58. McKinney JD, Bentrup KH, Muñoz-Elias EJ, Miczak A, Chen B, Chan WT et al. (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
59. Mickelsen PA, Sparling PF. (1981). Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds. Infect Immun 33: 555-564.
60. Miyamoto N, Yamamoto T, Yusa Y, Fujiwara Y. (2013). Postembryonic development of the bone-eating worm Osedax japonicus. Naturwissenschaften 100: 285-289.
61. Miyazaki M, Nogi Y, Fujiwara Y, Kawato M, Kubokawa K, Horikoshi K. (2008). Neptunomonas japonica sp. nov., an Osedax japonicus symbiont-like bacterium isolated from sediment adjacent to sperm whale carcasses off Kagoshima, Japan. Int J Syst Evol Microbiol 58: 866-871.
62. Monnet V. (2003). Bacterial oligopeptide-binding proteins. Cell Mol Life Sci 60: 2100-2114.
63. Muñoz-Elías EJ, McKinney JD. (2005). Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nature Med 11: 638-644.
64. Muñoz-Elías EJ, Upton AM, Cherian J, McKinney JD. (2006). Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60: 1109-1122.
65. Myers EW, Miller W. (1988). Optimal alignments in linear space. Comput Appl Biosci 4: 11-17.
66. Naganuma T, Elsaied HE, Hoshii D, Kimura H. (2005). Bacterial endosymbioses of gutless tube-dwelling worms in nonhydrothermal vent habitats. Mar Biotechnol 7: 416-428.
67. Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher CR et al. (2007). The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315: 998-1000.
68. Nussbaumer AD, Fisher CR, Bright M. (2006). Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441: 345-348.
69. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ et al. (2011). Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci USA 108: 11217-11222.
70. Oliveros JC. (2007). VENNYAn interactive tool for comparing lists with Venn Diagrams. http://bioinfogpcnbcsices/tools/venny/indexhtml.
71. Perry RD, Brubaker RR. (1979). Accumulation of iron by Yersiniae. J Bacteriol 137: 1290-1298.
72. Portnoy DA, Jacks PS, Hinrichs DJ. (1988). Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
73. Preusse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
74. Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T et al. (2008). Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10: 727-737.
75. Rouse GW, Goffredi SK, Vrijenhoek RC. (2004). Osedax: Bone-eating marine worms with dwarf males. Science 305: 668-671.
76. Rouse GW, Worsaae K, Johnson SB. (2008). Acquisition of dwarf male 'harems' by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biol Bull 214: 67-82.
77. Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC. (2011). Not whale-fall specialists, Osedax worms also consume fishbones. Biol Lett 7: 736-739.
78. Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R et al. (2005). Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102: 3004-3009.
79. Saitou N, Nei M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
80. SalathéRM, Vrijenhoek RC. (2012). Temporal variation and lack of host specificity among bacterial endosymbionts of Osedax bone worms (Polychaeta: Siboglinidae). BMC Evol Biol 12: 189.
81. Schell MA, Ulrich RL, RibotWJ, Brueggemann EE, Hines HB, Chen D et al. (2007). Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64: 1466-1485.
82. Schlieker C, Zentgraf H, Dersch P, Mogk A. (2005). ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem 386: 1115-1127.
83. Schwarz S, Hood RD, Mougous JD. (2010). What is type VI secretion doing in all those bugs? Trends Microbiol 18: 531-537.
84. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C. (2010). Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5: 61-70.
85. Smith CR, Baco AR. (2003). The ecology of whale-falls at the deep-sea floor. Oceanogr Mar Biol Annu Rev 41: 311-354.
86. Smith C, Baco A, Glover A. (2002). Faunal succession on replicate deep-sea whale-falls: time scales and ventseep affinities. Cah de Biolog Mar 43: 293-297.
87. Stoebner JA, Payne SM. (1988). Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect Immun 56: 2891-2895.
88. Sutherland WJ, Freckleton RP, Godfray HCJ, Beissinger SR, Benton T, Cameron DD et al. (2013). Identification of 100 fundamental ecological questions. J Ecol 101: 58-67.
89. Tatusov RL, Koonin EV, Lipman DJ. (1997). A genomic perspective on protein families. Science 278: 631-637.
90. Thompson JD, Gibson TJ, Higgins DG. (2002). Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2.
91. Thornhill DJ, Fielman KT, Santos SR, Halanych KM. (2008). Siboglinid-bacteria endosymbiosis: A model system for studying symbiotic mechanisms. Commun Integr Biol 1: 163-166.
92. Tomich M, Planet PJ, Figurski DH. (2007). The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5: 363-375.
93. Tresguerres M, Katz S, Rouse GW. (2013). How to get into bones: proton pump and carbonic anhydrase in Osedax boneworms. Proc Royal Soc B 280: 20130625.
94. Verna C, Ramette A, Wiklund H, Dahlgren TG, Glover AG, Gaill F et al. (2010). High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environ Microbiol 12: 2355-2370.
95. Vrijenhoek RC, Johnson SB, Rouse GW. (2008). Boneeating Osedax females and their 'harems' of dwarf males are recruited from a common larval pool. Molec Ecol 17: 4535-4544.
96. Vrijenhoek RC, Johnson SB, Rouse GW. (2009). A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biol 7: 74.
97. Wadhams GH, Armitage JP. (2004). Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
98. Warren MJ, Raux E, Schubert HL, Escalante-Semerena JC. (2002). The biosynthesis of adenosylcobalamin (Vitamin B12). Nat Prod Rep 19: 390-412.
99. Woyke T, Teeling H, Ivanova NN, Huntemann M, Richter M, Gloeckner FO et al. (2006). Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
100. Woyke T, Sczyrba A, Lee J, Rinke C, Tighe D, Clingenpeel S et al. (2011). Decontamination of MDA reagents for single cell whole genome amplification. PLoS One 6: e26161.
101. Yang JC, Madupu R, Durkin AS, Ekborg NA, Pedamallu CS, Hostetler JB et al. (2009). The complete genome of Teredinibacter turnerae T7901: an intracellular endosymbiont of marine wood-boring bivalves (shipworms). PLoS One 4: e6085.