Abstract
This study reports on the accumulation of iron within the tube wall of the deep sea vent macro invertebrate Vestimentiferan Ridgeia piscesae collected from Juan de Fuca ridge. Combining an array of approaches including environmental scanning electron microscope (ESEM), electron probe micro-analysis (EPMA), X-ray microanalysis (EDS) and transmission electron microscope (TEM), we provide evidences for the influence of prokaryotic organisms on the accumulation of metals on and within the tube wall. Two types of iron-rich minerals such as iron oxides and framboidal pyrites are identified within or on the tube wall. Our results reveal the presence of prokaryotic organism is apparently responsible for the early accumulation of iron-rich minerals in the tube wall. The implications of the biomineralisation of iron in tube wall at hydrothermal vents are discussed.
Similar content being viewed by others
References
Beveridge TJ, Fyfe WS (1985) Metal oxidation by bacterial cell walls. Can J Earth Sci 22:1892–1898
Beveridge TJ, Murray RGE (1980) Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol 141:876–887
Bottrell SH, Morton MDB (1992) A reinterpretation of the genesis of the Cae Coch pyrite deposit. N Wales J Geol Soc Lond 149:581–584
Cary SC, Warren W, Anderson E, Giovannoni SJ (1993) Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont-specific polymerase chain reaction amplification and in situ hybridization techniques. Mol Mar Biotechnol 2:51–62
Cavanaugh CM, Gardiner CL, Jones ML, Jannasch HW, Waterbury JB (1981) Procaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342. doi:10.1126/science.213.4505.340
Châtellier X, Fortin D, West M, Leppard GG, Ferris FG (2001) Effect of the presence of bacterial surfaces during the synthesis of Fe-oxides by oxidation of ferrous ions. Eur J Miner 13:705–714. doi:10.1127/0935-1221/2001/0013-0705
Châtellier X, West M, Rose J, Fortin D, Leppard GG, Ferris FG (2004) Oxidation of ferrous ions in the presence of various bacterial strains and inorganic ligands. Geomicrobiol J 21:99–112. doi:10.1080/01490450490266343
Cook TL, Stakes DS (1995) Biogeological mineralisation in deep-sea hydrothermal deposits. Science 267:1975–1979. doi:10.1126/science.267.5206.1975
Donald R, Southam G (1999) Low temperature anaerobic bacterial diagenesis of ferrous monosulfide to pyrite. Geoch Cosm Acta 63:2019–2023. doi:10.1016/S0016-7037(99)00140-4
Edwards KJ, Rogers DR, Wirsen CO, McCollom TM (2003) Isolation and characterization of novel psychrophilic neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Appl Environ Microbiol 69:2906–2913. doi:10.1128/AEM.69.5.2906-2913.2003
Edwards KJ, Bach W, McCollom TM, Rogers DR (2004) Neutrophilic Fe-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the deep-sea. Geomicrobiol J 21:393–404. doi:10.1080/01490450490485863
Edwards KJ, Bach W, McCollom TM (2005) Geomicrobiology in oceanography: microbe–mineral interactions at and below the seafloor. Trends Microbiol 13(9):449–456. doi:10.1016/j.tim.2005.07.005
Ehrlich HL (2002) Geomicrobiology of iron. In: Ehrlich HL (ed) Geomicrobiology. Marcel Dekker, Inc., New York, pp 345–428
Emerson D, Moyer CL (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792
Emerson D, Moyer CI (2002) Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl Environ Microbiol 68:3085–3093. doi:10.1128/AEM.68.6.3085-3093.2002
Emerson D, Weiss JV (2004) Bacterial iron oxidation in circumneutral freshwater habitats: findings from the field and the laboratory. Geomicrobiol J 21:405–414. doi:10.1080/01490450490485881
Fein JB, Scott S, Rivera N (2002) The effect of Fe and Si adsorption by Bacillus subtilis cell walls: insights into non-metabolic bacterial precipitation of silicate minerals. Chem Geol 182:265–273. doi:10.1016/S0009-2541(01)00294-7
Feldman RA, Black MB, Cary SC, Lutz RA, Vrijenhoek RC (1997) Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mol Mar Biol Biotechnol 6:268–277
Ferris FG, Fyfe WS, Beveridge TJ (1988) Metallic ion binding by bacillus subtilis: implications for the fossilization of microorganisms. Geology 16:149–152. doi:10.1130/0091-7613(1988)016<0149:MIBBBS>2.3.CO;2
Folk RL (2005) Nannobacteria and the formation of framboidal pyrite: textural evidence. J Earth Syst Sci 114(3):369–374. doi:10.1007/BF02702955
Fortin D, Langley S (2005) Formation and occurrence of biogenic iron-rich minerals. Earth Sci Rev 72:1–19. doi:10.1016/j.earscirev.2005.03.002
Gaill F, Hunt S (1986) Tubes of deep sea hydrothermal vent worms Riftia pachyptila (Vestimentifera) and Alvinella pompejana (Annelida). Mar Ecol Prog Ser 34:267–274. doi:10.3354/meps034267
Gaill F, Hunt S (1991) The biology of annelid worms from high temperature hydrothermal vent regions. Rev Aquat Microbiol 4:107–137
Garcia-Guinea J, Martinez-Frias J, Gonzales-Martin R, Zamora L (1997) Framboidal pyrites in antique books. Nature 388:631. doi:10.1038/41677
Hallberg R, Ferris FG (2004) Biomineralization by Gallionella. Geomicrobiol J 21:325–330. doi:10.1080/01490450490454001
Holden JF, Adams MWW (2003) Microbe-metal interactions in marine hydrothermal environments. Curr Opin Chem Biol 7:160–165. doi:10.1016/S1367-5931(03)00026-7
Jonasson IR, Walker DA (1987) Micro-organisms and their debris as substrates for base metal sulfide ucleation and accumulation in some mid-ocean ridge deposits. Eos Trans AGU 68:1546
Jones ML (1985) On the vestimentifera, new phylum: six species, and other taxa, from hydrothermal vents and elsewhere. Bull Biol Soc Wash 6:117–158
Juniper SK, Tebo BM (1995) Microbe-metal interactions and mineral deposition at hydrothermal vents. In: Karl DM (ed) The Microbiology of Deep-Sea Hydrothermal Vents. CRC Press, Boca Raton, FL, pp 219–253
Kádár E, Bettencourt R (2008) Ultrastructural and molecular evidence for potentially symbiotic bacteria within the byssal plaques of the deep-sea hydrothermal vent mussel Bathymodiolus azoricus. Biometals 21:395–404. doi:10.1007/s10534-007-9128-1
Kádár E, Costa V, Martins I, Santos RS, Powell JJ (2005) Enrichment in trace metals of macro-invertebrate habitats at hydrothermal vents along the mid Atlantic Ridge. Hydrobiologia 548:191–205. doi:10.1007/s10750-005-4758-1
Kádár E, Costa V, Santos RS, Powell JJ (2006a) Tissue partitioning of micro-essential metals in the vent bivalve Bathymodiolus azoricus and associated organisms (endosymbiont bacteria and parasite polychaete) from geochemically distinct vents of the mid-Atlantic Ridge. J Sea Res 56:45–52. doi:10.1016/j.seares.2006.01.002
Kádár E, Costa V, Santos RS (2006b) Distribution of microessential (Fe, Cu, Zn) and toxic (Hg) metals in tissues of two nutritionally distinct hydrothermal shrimps. Sci Total Environ 358:143–150. doi:10.1016/j.scitotenv.2005.09.003
Kádár E, Santos RS, Powell JJ (2006c) Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the mid-Atlantic Ridge. Environ Res 101:221–229. doi:10.1016/j.envres.2005.08.010
Kelley DS, Baross JA, Delaney JR (2002) Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu Rev Earth Planet Sci 30:385–491. doi:10.1146/annurev.earth.30.091201.141331
Konhauser KO (1998) Diversity of bacterial iron mineralization. Earth Sci Rev 43:91–121. doi:10.1016/S0012-8252(97)00036-6
Lane DJ, Stahl DA, Olsen GJ, Pace NR (1985) Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Bull Biol Soc Wash 6:389–400
Little CTS, Glynn SEJ, Mills RA (2004) Four-hundred-andninty-million-year record of bacterial iron oxide precipitation at sea-floor hydrothermal vents. Geomicrobiol J 25:415–429. doi:10.1080/01490450490485845
Love LG, Al-Kaisy, Adil TH, Brockley Harry (1984) Mineral and organic material in matrices and coatings of framboidal pyrite from Pennsylvanian sediments. Engl J Sed Petr 54:869–876
Maginn EJ, Little CTS, Herrington RJ, Mills RA (2002) Sulphide mineralisation in the deep sea hydrothermal vent polychaete, Alvinella pompejana: implications for fossil preservation. Mar Geol 181:337–356. doi:10.1016/S0025-3227(01)00196-7
Posfai M, Buseck PR, Bazylinski DA, Frankel RB (1998) Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science 280:880–883. doi:10.1126/science.280.5365.880
Reysenbach AL, Shock ES (2002) Merging genomes with geochemistry in hydrothermal ecosystems. Science 296:1077–1082. doi:10.1126/science.1072483
Southward EC, Tunnicliffe V, Black M (1995) Revision of the species of Ridgeia from northeast Pacific hydrothermal vents, with a redescription of Ridgeia piscesae Jones (Pogonophora: Obturata = Vestimentifera). Can J Zool 73:282–295. doi:10.1139/z95-033
Suzuki Y, Kopp RE, Kogure T, Suga A, Takai K (2006) Sclerite formation in the hydrothermal-vent “scaly-foot” gastropod: possible control of iron sulfide biomineralization by the animal. Earth Planet Sci Lett 242:39–50. doi:10.1016/j.epsl.2005.11.029
Tunnicliffe V, Fontaine AR (1987) Faunal composition and organic surface encrustations at hydrothermal vents on the southern Juan de Fuca Ridge. J Geophys Res 92:11303–11314. doi:10.1029/JB092iB11p11303
Urcuyo IA, Massoth GJ, Julian D, Fisher CR (2003) Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge. Deep-Sea Res 50(Pt I):763–780. doi:10.1016/S0967-0637(03)00061-X
Verati C, de Donato P, Prieur D, Lancelot J (1999) Evidence of bacterial activity from micrometer-scale layer analyses of black-smoker sulfide structures (Pito Seamount Site, Easter microplate). Chem Geol 158:257–269. doi:10.1016/S0009-2541(99)00054-6
Zbinden M, Le Bris N, Gaill F, Compere P (2004) Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog Ser 284:237–251. doi:10.3354/meps284237
Acknowledgments
The authors are indebted to Dr. Maurice Tivey and Prof. Marvin Lilley for their kindly help during the sample collection. We thank the constructive remarks made by two anonymous reviewers. Special thanks also go to all the participants of the joint China and US submersible dive expedition cruise.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Peng, X., Zhou, H., Yao, H. et al. Ultrastructural evidence for iron accumulation within the tube of Vestimentiferan Ridgeia piscesae . Biometals 22, 723–732 (2009). https://doi.org/10.1007/s10534-009-9216-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-009-9216-5