Microbial diversity in Frenulata (Siboglinidae, Polychaeta) species from mud volcanoes in the Gulf of Cadiz (NE Atlantic)

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 100, Issue 1, 2011, Pages 83-98

  Rodrigues, Clara F ^a   Hilário, Ana ^a   Cunha, Marina R ^a   Weightman, Andrew J ^b   Webster, Gordon ^b,c  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Bacteria; Frenulata; Gulf of Cadiz; Siboglinidae

Indexed keywords

RNA 16S;

ARTICLE; ATLANTIC OCEAN; BACTERIAL GENE; FRENULATA; GAMMAPROTEOBACTERIA; MARINE SPECIES; METHANOTROPHIC BACTERIUM; MICROBIAL DIVERSITY; MICROFLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLUM; POLYCHAETA; PRIORITY JOURNAL; SYMBIOSIS; UNINDEXED SEQUENCE; VOLCANO;

ANIMALS; ATLANTIC OCEAN; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYCHAETA; SEAWATER; SYMBIOSIS;

ANNELIDA; BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; INVERTEBRATA; PERVIATA; POLYCHAETA; SIBOGLINIDAE;

EID: 79958776157     PISSN: 00036072     EISSN: 15729699     Source Type: Journal    
DOI: 10.1007/s10482-011-9567-0     Document Type: Article

References (53)

1. Arp AJ, Childress JJ (1981) Blood function in the hydrothermal vent vestimentiferan tube worm. Science 213:342-344
2. Ball AD, Purdy KJ, Glover EA, Taylor JD (2009) Ctenidial structure and three bacterial symbiont morphotype in Anodontia (Euanodontia) ovum (Reeve, 1850) from the great barrier reef, Australia (Bivalvia: Lucinidae). J Mollus Stud 75:175-185
3. Callsen-Cencic P, Flügel HJ (1995) Larval development and the formation of the gut of Siboglinum poseidoni Flügel & Langhof (Pogonophora, Perviata). Evidence of protostomian affinity. Sarsia 80:73-89
4. Caullery M (1914) Sur les Siboglinidae, type nouveau d'in- vertébrés receuillis par l'expédition du Siboga. CR Acad Sci III Vie 158:2014-2017
5. Cavanaugh CM (1985) Symbiosis of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Biol Soc Wash Bull 6:373-388
6. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm, Riftia pachyptila: possible chemoautotrophic symbionts. Science 213:340-342
7. Chao LSL, Davis RE, Moyer CL (2007) Characterization of bacterial community structure in vestimentiferan tube-worm Ridgeia piscesae trophosomes. Mar Ecol 28:72-85 (Pubitemid 46390356)
8. Childress JJ, Arp AJ, Fisher CR (1984) Metabolic blood characteristics of the hydrothermal vent tube-worm Riftia pachyptila. Mar Biol 83:109-124
9. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259-2261 (Pubitemid 350031697)
10. Cunha MR, Hilário A, Teixeira IG (2001) The faunal community associated to mud volcanoes in the Gulf of Cadiz. In: Geological Processes on Deep-Water European Margins. IOC Workshop Report 175, p. 62
11. Di Meo CA, Wilbur AE, Holben WE, Feldman RA, Vrijenhoek RC, Cary CS (2000) Genetic variation among endosymbionts of widely distributed vestimentiferan tube-worms. Appl Environ Microbiol 66:651-658 (Pubitemid 30082754)
12. Duperron S, de Beer D, Zbinden M, Boetius A, Schipani V, Kahil N, Gaill F (2009) Molecular characterization of bacteria associated with the trophosome and the tube of Lamellibrachia sp., a siboglinid annelid from cold seeps in the eastern Mediterranean. FEMS Microbiol Ecol 69:395-409
13. Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tubeworm. Riftia pachyptila Jones (Vestimentifera). Science 213:336-338
14. Fry JC, Webster G, Cragg BA, Weightman AJ, Parkes RJ (2006) Analysis of DGGE profiles to explore the relationship between prokaryotic diversity and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 58:86-98 (Pubitemid 44359310)
15. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R, Vrinjenhoek RC (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7:1369-1378 (Pubitemid 41204931)
16. 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 (Pubitemid 46649524)
17. Gulledge J, Ahmad A, Steudler PA, Pomeranzt WJ, Cavanaugh C (2001) Family- and Genus-level 16S rRNA-targeted oligonucleotide probes for ecological studies of methanotrophic bacteria. Appl Environ Microbiol 67(10):4726-4733 (Pubitemid 33646106)
18. Halanych KM (2005) Molecular phylogeny of siboglinid annelids (a.k.a. pogonophorans): a review. Hydrobiologia 535:297-307
19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
20. Hilário A, Cunha MR (2008) On some frenulate species (Annelida: Polychaeta: Siboglinidae) from mud volcanoes in the Gulf of Cadiz (NE Atlantic). Sci Mar 72(2):361-371
21. Hilário A, Capa M, Dahlgren TG, Halanych KM, Little CTS, Thornhill DJ, Verna C, Glover AG (2011) New perspectives on the ecology and evolution of siboglinid tubeworms. PLoS ONE 6:e16309. doi:10.1371/journal.pone.0016309
22. Hilário A, Johnson SB, Cunha MR, Vrijenhoek RC (2010) High diversity of frenulates (Polychaeta: Siboglinidae) in the Gulf of Cadiz mud volcanoes: a DNA taxonomy analysis. Deep Sea Res I 57:143-150
23. Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203-208
24. Kimura H, Higashide Y, Naganuma T (2003) Endosymbiotic microflora of the vestimentiferan tubeworm Lamellibrachia sp.) from a bathyal cold seep. Mar Biotechonol 5:593-603 (Pubitemid 38106643)
25. Kubota N, Kanemori M, Sasayama Y, Aida M, Fukumori Y (2007) Identification of endosymbionts in Oligobrachia mashikoi (Siboglinidae, Annelida). Microbes Environ 22:136-144
26. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stakebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115-175
27. Lazar CS, Dinasquet J, Pignet P, Prieur D, Toffin L (2010) Active archaeal communities at cold seeps sediments populated by Siboglinidae tubeworms from the Storegga Slide. Microbiol Ecol 60:516-527
28. Lösekann T, Robador A, Niemann H, Knittel K, Boetius A, Dubilier N (2008) Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby Mud Volcano, Barents Sea). Environ Microbiol 10:3237-3254
29. McMullin ER, Hourdez S, Schaeffer SW, Fisher CR (2003) Phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34:1-41 (Pubitemid 36280641)
30. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700 (Pubitemid 23072343)
31. Nelson K, Fisher CR (2000) Speciation of the bacterial symbionts of deep-sea vestimentiferan tube worms. Symbiosis 28:1-15 (Pubitemid 30221200)
32. O'Sullivan LA, Webster G, Fry JC, Parkes RJ, Weightman AJ (2008) Modified linker-PCR facilitate complete sequencing of DGGE DNA fragments. J Microbiol Methods 75:579-581
33. Redmond MC, Valentine DL, Sessions AL (2010) Identification of novel methane-, ethane-, and propane-oxidizing bacteria at marine hydrocarbon seeps by stable isotope probing. Appl Environ Microbiol 76:6412-6422
34. Reed AJ, Dorn R, Van Dover CL, Lutz RA, Vetriani C (2009) Phylogenetic diversity of methanogenic, sulfate-reducing and methanotrophic prokaryotes from deep-sea hydrothermal vents and cold seeps. Deep Sea Res II 56:1665-1674
35. Rodrigues C, Cunha MR (2005) Common chemosynthetic species in the Gulf of Cadiz: updated spatial distribution. In: Geological processes on deep-water European margins, IOC Workshop Report 197, pp 26-28
36. Rodrigues CF, Webster G, Cunha MR, Duperron S, Weightman AJ (2010) Chemosynthetic bacteria found in bivalve species from mud volcanoes of the Gulf of Cadiz. FEMS Microbiol Ecol 73:486-499
37. Schloss PD, Handelsmann J (2004) Status of the microbial census. Microbiol Mol Biol Rev 68:686-691 (Pubitemid 39628533)
38. Schmaljohann R (1991) Oxidation of various potential energy sources by methanotrophic endosymbionts of Siboglinum poseidoni (Pogonophora). Mar Ecol Prog Ser 76:143-148
39. Schmaljohann R, Flügel HJ (1987) Methane-oxidizing bacteria in Pogonophora. Sarsia 72:91-98
40. Schmaljohann R, Faber E, Whiticar MJ, Dando PR (1990) Co-existence of methane- and sulphur-based endosymbioses between bacteria and invertebrates at a site in the Skagerrak. Mar Ecol Prog Ser 61:119-124
41. Southward EC (1982) Bacterial symbionts in Pogonophora. J Mar Biol Ass UK 62:889-906
42. Southward AJ, Southward EC, Dando PR, Barrett RL, Ling R (1986) Chemoautotrophic function of bacterial symbionts in small pogonophora. J Mar Biol Ass UK 66:415-437
43. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599 (Pubitemid 47236692)
44. Tavormina PL, Ussler W, Orphan VJ (2008) Planktonic and sediment-associated aerobic methanotrophs in two seep systems along the North American margin. Appl Environ Microbiol 74:3985-3995 (Pubitemid 351962423)
45. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X-Windows interface: flexible strategies for multiple sequence alignments aided by quality analysis tools. Nucleic Acids Res 25:4876-4882 (Pubitemid 28022245)
46. Thornhill DJ, Wiley AA, Campbell AL, Bartol FF, Teske A, Halanych KM (2008a) Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida). Biol Bull 214:135-144 (Pubitemid 351581375)
47. Thornhill DJ, Fielman KT, Santos SR, Halanych KM (2008b) Siboglinid-bacteria endosymbiosis: a model system for studying symbiotic mechanisms. Commun Integr Biol 1:1-4
48. Vanreusel A, Andersen AC, Boetius A, Connelly D, Cunha MR, Decker C, Hilário A, Kormas KA, Maignien L, Olu K, Pachiadaki M, Ritt B, Rodrigues CF, Sarrazin J, Tyler PA, Van Gaever S, Vanneste H (2009) Biodiversity of cold seep ecosystems along the european margins. Oceanography 22:110-127
49. Verna C, Ramette A, Wiklund H, Dahlgren TG, Glover AG, Gaill F, Dubilier N (2010) High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environ Microbiol 12:2355-2370
50. Vrijenhoek RC, Duhaime M, Jones WJ (2007) Subtype variation among bacterial endosymbionts of tubeworms (Annelida: Siboglinidae) from the Gulf of California. Biol Bull 212:180-184 (Pubitemid 46988410)
51. Webster G, Parkes RJ, Cragg BA, Newberry CJ, Weightman AJ, Fry JC (2006) Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 58:65-85 (Pubitemid 44359309)
52. Webster G, Yarram L, Freese E, Koster J, Sass J, Parkes RJ, Weightman AJ (2007) Distribution of candidate division JS1 and other Bacteria in tidal sediments of the German Wadden Sea using targeted 16S rRNA gene PCR-DGGE. FEMS Microbiol Ecol 62:78-89 (Pubitemid 47515204)
53. Won Y, Hallam SJ, Mullan GD, Pan I, Buck KR, Vrijenhoek R (2003) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the Genus Bathymodiolus. Appl Environ Microbiol 69:6785-6792 (Pubitemid 37420218)