Cited by 63Microbial Community Ecology and PhysiologyMethane Hydrates and Related PhenomenaMarine Biology and Ecology Research

Functional interactions among filamentous E psilonproteobacteria and B acteroidetes in a deep‐sea hydrothermal vent biofilm

Open access
Stokke, Runar, Dahle, Håkon, Roalkvam, Irene, Wissuwa, Juliane, Daae, Frida Lise, Tooming‐Klunderud, Ave, Thorseth, Ingunn H., Pedersen, Rolf B. +1 more·2015·Environmental Microbiology

Abstract

Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in the Loki's Castle vent field. Imaging revealed the presence of rod-shaped Bacteroidetes growing as ectobionts on long, sheathed microbial filaments (> 100 μm) affiliated with the Sulfurovum genus within Epsilonproteobacteria. The filaments were composed of a thick (> 200 nm) stable polysaccharide, representing a substantial fraction of organic carbon produced by primary production. An integrated -omics approach enabled us to assess the metabolic potential and in situ metabolism of individual taxonomic and morphological groups identified by imaging. Specifically, we provide evidence that organotrophic Bacteroidetes attach to and glide along the surface of Sulfurovum filaments utilizing organic polymers produced by the lithoautotrophic Sulfurovum. Furthermore, in situ expression of acetyl-CoA synthetase by Sulfurovum suggested the ability to assimilate acetate, indicating recycling of organic matter in the biofilm. This study expands our understanding of the lifestyles of Epsilonproteobacteria in hydrothermal vents, their metabolic properties and co-operative interactions in deep-sea hydrothermal vent food webs.

Integrity signals

Registry

Crossref · 10.1111/1462-2920.12970

Cites

83 of 83 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

The text we found for this paper looks like another document, so its claims and self-check weren’t run. The registry and citation checks still apply.

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The text we found for this paper looks like another document, so the self-check wasn’t run.

Cites

Flagged first, then by citations

Research works printed but not linked: 116

  1. Adrio, J. L. and A. L. Demain (2014). "Microbial enzymes: tools for biotechnological processes." Biomolecules 4(1): 117-139.
  2. Albertsen, M., P. Hugenholtz, A. Skarshewski, K. L. Nielsen, G. W. Tyson and P. H. Nielsen (2013). "Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes." Nat Biotechnol 31(6): 533-538.
  3. Angiuoli, S. V., A. Gussman, W. Klimke, G. Cochrane, D. Field, G. Garrity, C. D. Kodira, N. Kyrpides, R. Madupu, V. Markowitz, et al. (2008). "Toward an online repository of Standard Operating Procedures (SOPs) for (meta)genomic annotation." OMICS 12(2): 137-141.
  4. Bayer, E. A., E. Morag and R. Lamed (1994). "The cellulosome--a treasure-trove for biotechnology." Trends Biotechnol 12(9): 379-386.
  5. Beja, O., L. Aravind, E. V. Koonin, M. T. Suzuki, A. Hadd, L. P. Nguyen, S. B. Jovanovich, C. M. Gates, R. A. Feldman, J. L. Spudich, et al. (2000a). "Bacterial rhodopsin: evidence for a new type of phototrophy in the sea." Science 289(5486): 1902-1906.
  6. Beja, O., M. T. Suzuki, E. V. Koonin, L. Aravind, A. Hadd, L. P. Nguyen, R. Villacorta, M. Amjadi, C. Garrigues, S. B. Jovanovich, et al. (2000b). "Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage." Environ Microbiol 2(5): 516- 529.
  7. Bell, G. S., R. J. Russell, H. Connaris, D. W. Hough, M. J. Danson and G. L. Taylor (2002). "Stepwise adaptations of citrate synthase to survival at life's extremes. From psychrophile to hyperthermophile." Eur J Biochem 269(24): 6250-6260.
  8. Bentley, D. R., S. Balasubramanian, H. P. Swerdlow, G. P. Smith, J. Milton, C. G. Brown, K. P. Hall, D. J. Evers, C. L. Barnes, H. R. Bignell, et al. (2008). "Accurate whole human genome sequencing using reversible terminator chemistry." Nature 456(7218): 53-59.
  9. Biver, S., A. Stroobants, D. Portetelle and M. Vandenbol (2014). "Two promising alkaline beta- glucosidases isolated by functional metagenomics from agricultural soil, including one showing high tolerance towards harsh detergents, oxidants and glucose." J Ind Microbiol Biotechnol 41(3): 479- 488.
  10. Biwer, A., G. Antranikian and E. Heinzle (2002). "Enzymatic production of cyclodextrins." Appl Microbiol Biotechnol 59(6): 609-617.
  11. Brandelli, A. (2008). "Bacterial Keratinases: Useful Enzymes for Bioprocessing Agroindustrial Wastes and Beyond." Food and Bioprocess Technology 1(2): 105-116.
  12. Cavicchioli, R., R. Amils, D. Wagner and T. McGenity (2011a). "Life and applications of extremophiles." Environ Microbiol 13(8): 1903-1907.
  13. Cavicchioli, R., T. Charlton, H. Ertan, S. Mohd Omar, K. S. Siddiqui and T. J. Williams (2011b). "Biotechnological uses of enzymes from psychrophiles." Microb Biotechnol 4(4): 449-460.
  14. Cherry, J. R. and A. L. Fidantsef (2003). "Directed evolution of industrial enzymes: an update." Curr Opin Biotechnol 14(4): 438-443.
  15. Chevreux, B., T. Pfisterer, B. Drescher, A. J. Driesel, W. E. Muller, T. Wetter and S. Suhai (2004). "Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs." Genome Res 14(6): 1147-1159.
  16. Choi, D. H. and B. C. Cho (2006). "Lutibacter litoralis gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from tidal flat sediment." International journal of systematic and evolutionary microbiology 56(Pt 4): 771-776.
  17. Coorevits, A., A. E. Dinsdale, G. Halket, L. Lebbe, P. De Vos, A. Van Landschoot and N. A. Logan (2012). "Taxonomic revision of the genus Geobacillus: emendation of Geobacillus, G. stearothermophilus, G. jurassicus, G. toebii, G. thermodenitrificans and G. thermoglucosidans (nom. corrig., formerly 'thermoglucosidasius'); transfer of Bacillus thermantarcticus to the genus as G. thermantarcticus comb. nov.; proposal of Caldibacillus debilis gen. nov., comb. nov.; transfer of G. tepidamans to Anoxybacillus as A. tepidamans comb. nov.; and proposal of Anoxybacillus caldiproteolyticus sp. nov." Int J Syst Evol Microbiol 62(7): 1470-1485.
  18. Corliss, J. B., J. Dymond, L. I. Gordon, J. M. Edmond, R. P. V. Herzen, R. D. Ballard, K. Green, D. Williams, A. Bainbridge, K. Crane, et al. (1979). "Submarine Thermal Springs on the Galapagos Rift." Science 203(4385): 1073-1083.
  19. Crabb, W. D. and J. K. Shetty (1999). "Commodity scale production of sugars from starches." Curr Opin Microbiol 2(3): 252-256.
  20. Craig, J. W., F. Y. Chang, J. H. Kim, S. C. Obiajulu and S. F. Brady (2010). "Expanding small- molecule functional metagenomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse Proteobacteria." Appl Environ Microbiol 76(5): 1633-1641.
  21. D'Amico, S., C. Gerday and G. Feller (2003). "Temperature adaptation of proteins: engineering mesophilic-like activity and stability in a cold-adapted alpha-amylase." J Mol Biol 332(5): 981-988.
  22. Dalmaso, G. Z., D. Ferreira and A. B. Vermelho (2015). "Marine extremophiles: a source of hydrolases for biotechnological applications." Mar Drugs 13(4): 1925-1965.
  23. De Santi, C., B. Altermark, D. de Pascale and N. P. Willassen (2016a). "Bioprospecting around Arctic islands: Marine bacteria as rich source of biocatalysts." J Basic Microbiol 56(3): 238-253.
  24. De Santi, C., B. Altermark, M. M. Pierechod, L. Ambrosino, D. de Pascale and N. P. Willassen (2016b). "Characterization of a cold-active and salt tolerant esterase identified by functional screening of Arctic metagenomic libraries." BMC Biochem 17(1): 1.
  25. Demain, A. L. and J. L. Adrio (2008). "Contributions of microorganisms to industrial biology." Mol Biotechnol 38(1): 41-55.
  26. Donk, P. J. (1920). "A Highly Resistant Thermophilic Organism." J Bacteriol 5(4): 373-374.
  27. Dubilier, N., C. Bergin and C. Lott (2008). "Symbiotic diversity in marine animals: the art of harnessing chemosynthesis." Nat Rev Microbiol 6(10): 725-740.
  28. Eid, J., A. Fehr, J. Gray, K. Luong, J. Lyle, G. Otto, P. Peluso, D. Rank, P. Baybayan, B. Bettman, et al. (2009). "Real-time DNA sequencing from single polymerase molecules." Science 323(5910): 133-138.
  29. Ekkers, D. M., M. S. Cretoiu, A. M. Kielak and J. D. Elsas (2012). "The great screen anomaly--a new frontier in product discovery through functional metagenomics." Appl Microbiol Biotechnol 93(3): 1005-1020.
  30. Feller, G. (2010). "Protein stability and enzyme activity at extreme biological temperatures." J Phys Condens Matter 22(32): 323101.
  31. Ferrer, M., A. Beloqui, K. N. Timmis and P. N. Golyshin (2009). "Metagenomics for mining new genetic resources of microbial communities." J Mol Microbiol Biotechnol 16(1-2): 109-123.
  32. Flores, G. E., J. H. Campbell, J. D. Kirshtein, J. Meneghin, M. Podar, J. I. Steinberg, J. S. Seewald, M. K. Tivey, M. A. Voytek, Z. K. Yang, et al. (2011). "Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge." Environ Microbiol 13(8): 2158-2171.
  33. Flores, G. E. and A. L. Reysenbach (2011). Hydrothermal Environments, Marine. Encyclopedia of Geobiology. Netherlands, Springer: 456-467.
  34. Fullwood, M. J., C. L. Wei, E. T. Liu and Y. Ruan (2009). "Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses." Genome Res 19(4): 521-532.
  35. Giardina, T., A. P. Gunning, N. Juge, C. B. Faulds, C. S. Furniss, B. Svensson, V. J. Morris and G. Williamson (2001). "Both binding sites of the starch-binding domain of Aspergillus niger glucoamylase are essential for inducing a conformational change in amylose." J Mol Biol 313(5): 1149-1159.
  36. Gonzalez, J. M., B. Fernandez-Gomez, A. Fernandez-Guerra, L. Gomez-Consarnau, O. Sanchez, M. Coll-Llado, J. Del Campo, L. Escudero, R. Rodriguez-Martinez, L. Alonso-Saez, et al. (2008). "Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria)." Proc Natl Acad Sci U S A 105(25): 8724-8729.
  37. Guillen, D., S. Sanchez and R. Rodriguez-Sanoja (2010). "Carbohydrate-binding domains: multiplicity of biological roles." Appl Microbiol Biotechnol 85(5): 1241-1249.
  38. Gupta, R., R. Rajput, R. Sharma and N. Gupta (2013). "Biotechnological applications and prospective market of microbial keratinases." Appl Microbiol Biotechnol 97(23): 9931-9940.
  39. Handelsman, J., M. R. Rondon, S. F. Brady, J. Clardy and R. M. Goodman (1998). "Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products." Chem Biol 5(10): R245-249.
  40. Healy, F. G., R. M. Ray, H. C. Aldrich, A. C. Wilkie, L. O. Ingram and K. T. Shanmugam (1995). "Direct isolation of functional genes encoding cellulases from the microbial consortia in a thermophilic, anaerobic digester maintained on lignocellulose." Appl Microbiol Biotechnol 43(4): 667-674.
  41. Huber, J. A., D. A. Butterfield and J. A. Baross (2003). "Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption." FEMS Microbiol Ecol 43(3): 393-409.
  42. Izquierdo, J. A., L. Goodwin, K. W. Davenport, H. Teshima, D. Bruce, C. Detter, R. Tapia, S. Han, M. Land, L. Hauser, et al. (2012). "Complete Genome Sequence of Clostridium clariflavum DSM 19732." Stand Genomic Sci 6(1): 104-115.
  43. Jaeschke, A., S. L. Jorgensen, S. M. Bernasconi, R. B. Pedersen, I. H. Thorseth and G. L. Fruh- Green (2012). "Microbial diversity of Loki's Castle black smokers at the Arctic Mid-Ocean Ridge." Geobiology 10(6): 548-561.
  44. Janecek, S., B. Svensson and E. A. MacGregor (2011). "Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals." Enzyme Microb Technol 49(5): 429-440.
  45. Janecek, S., B. Svensson and E. A. MacGregor (2014). "alpha-Amylase: an enzyme specificity found in various families of glycoside hydrolases." Cell Mol Life Sci 71(7): 1149-1170.
  46. Jorgensen, S. L., B. Hannisdal, A. Lanzen, T. Baumberger, K. Flesland, R. Fonseca, L. Ovreas, I. H. Steen, I. H. Thorseth, R. B. Pedersen, et al. (2012). "Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge." Proc Natl Acad Sci U S A 109(42): E2846-2855.
  47. Kakirde, K. S., L. C. Parsley and M. R. Liles (2010). "Size does matter: Application-driven approaches for soil metagenomics." Soil Biology & Biochemistry 42(11): 1911-1923.
  48. Kasana, R. C., R. Salwan, H. Dhar, S. Dutt and A. Gulati (2008). "A Rapid and Easy Method for the Detection of Microbial Cellulases on Agar Plates Using Gram's Iodine." Current Microbiology 57(5): 503-507.
  49. Kelley, D. S., J. A. Baross and J. R. Delaney (2002). "Volcanoes, fluids, and life at mid-ocean ridge spreading centers." Annual Review of Earth and Planetary Sciences 30: 385-491.
  50. Kelly, R. M., L. Dijkhuizen and H. Leemhuis (2009). "Starch and alpha-glucan acting enzymes, modulating their properties by directed evolution." J Biotechnol 140(3-4): 184-193.
  51. Kennedy, J., B. Flemer, S. A. Jackson, D. P. Lejon, J. P. Morrissey, F. O'Gara and A. D. Dobson (2010). "Marine metagenomics: new tools for the study and exploitation of marine microbial metabolism." Mar Drugs 8(3): 608-628.
  52. Kindle, K. L., S. E. Mainzer, D. L. Marlatt and C. B. Sawyer (1986). Thermostable alpha amylase having a low requirement for calcium ions, derived from a Bacillus microorganism. Corning Glass Works. US, Google Patents, US4600693 A Knapp, S., S. Kardinahl, N. Hellgren, G. Tibbelin, G. Schafer and R. Ladenstein (1999). "Refined crystal structure of a superoxide dismutase from the hyperthermophilic archaeon Sulfolobus acidocaldarius at 2.2 A resolution." J Mol Biol 285(2): 689-702.
  53. Lammle, K., H. Zipper, M. Breuer, B. Hauer, C. Buta, H. Brunner and S. Rupp (2007). "Identification of novel enzymes with different hydrolytic activities by metagenome expression cloning." J Biotechnol 127(4): 575-592.
  54. Lange, L., Y. Huang and P. K. Busk (2016). "Microbial decomposition of keratin in nature-a new hypothesis of industrial relevance." Appl Microbiol Biotechnol 100(5): 2083-2096.
  55. Lanzen, A., S. L. Jorgensen, M. M. Bengtsson, I. Jonassen, L. Ovreas and T. Urich (2011). "Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA." FEMS Microbiol Ecol 77(3): 577-589.
  56. Le Moine Bauer, S., I. Roalkvam, I. H. Steen and H. Dahle (in review). "Lutibacter profundi sp. nov., isolated from a deep-sea hydrothermal system on the Arctic mid-ocean ridge." International Journal of Systematic and Evolutionary Microbiology in Revision.
  57. Lee, H. S., M. S. Kim, H. S. Cho, J. I. Kim, T. J. Kim, J. H. Choi, C. Park, H. S. Lee, B. H. Oh and K. H. Park (2002). "Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other." J Biol Chem 277(24): 21891-21897.
  58. Levasseur, A., E. Drula, V. Lombard, P. M. Coutinho and B. Henrissat (2013). "Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes." Biotechnol Biofuels 6(1): 41.
  59. Liu, Y., Y. Lei, X. Zhang, Y. Gao, Y. Xiao and H. Peng (2012b). "Identification and phylogenetic characterization of a new subfamily of alpha-amylase enzymes from marine microorganisms." Mar Biotechnol (NY) 14(3): 253-260.
  60. MacGregor, E. A. and B. Svensson (1989). "A super-secondary structure predicted to be common to several alpha-1,4-D-glucan-cleaving enzymes." Biochem J 259(1): 145-152.
  61. Mallick, P., D. R. Boutz, D. Eisenberg and T. O. Yeates (2002). "Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds." Proc Natl Acad Sci U S A 99(15): 9679-9684.
  62. Marcy, Y., C. Ouverney, E. M. Bik, T. Losekann, N. Ivanova, H. G. Martin, E. Szeto, D. Platt, P. Hugenholtz, D. A. Relman, et al. (2007). "Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth." Proc Natl Acad Sci U S A 104(29): 11889-11894.
  63. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y. J. Chen, Z. T. Chen, et al. (2005). "Genome sequencing in microfabricated high- density picolitre reactors." Nature 437(7057): 376-380.
  64. Maruthamuthu, M., D. J. Jimenez, P. Stevens and J. D. van Elsas (2016). "A multi-substrate approach for functional metagenomics-based screening for (hemi)cellulases in two wheat straw- degrading microbial consortia unveils novel thermoalkaliphilic enzymes." BMC Genomics 17(1): 86.
  65. McLean, B. W., A. B. Boraston, D. Brouwer, N. Sanaie, C. A. Fyfe, R. A. Warren, D. G. Kilburn and C. A. Haynes (2002). "Carbohydrate-binding modules recognize fine substructures of cellulose." J Biol Chem 277(52): 50245-50254.
  66. Michalska, K., A. D. Steen, G. Chhor, M. Endres, A. T. Webber, J. Bird, K. G. Lloyd and A. Joachimiak (2015). "New aminopeptidase from "microbial dark matter" archaeon." FASEB J 29(9): 4071-4079.
  67. Michel, G., T. Barbeyron, B. Kloareg and M. Czjzek (2009). "The family 6 carbohydrate-binding modules have coevolved with their appended catalytic modules toward similar substrate specificity." Glycobiology 19(6): 615-623.
  68. Moyer, C. L., F. C. Dobbs and D. M. Karl (1995). "Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii." Appl Environ Microbiol 61(4): 1555-1562.
  69. Neveu, J., C. Regeard and M. S. DuBow (2011). "Isolation and characterization of two serine proteases from metagenomic libraries of the Gobi and Death Valley deserts." Appl Microbiol Biotechnol 91(3): 635-644.
  70. Orcutt, B. N., J. B. Sylvan, N. J. Knab and K. J. Edwards (2011). "Microbial ecology of the dark ocean above, at, and below the seafloor." Microbiol Mol Biol Rev 75(2): 361-422.
  71. Park, B. H., T. V. Karpinets, M. H. Syed, M. R. Leuze and E. C. Uberbacher (2010). "CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database." Glycobiology 20(12): 1574-1584.
  72. Peng, H., Y. Zheng, M. Chen, Y. Wang, Y. Xiao and Y. Gao (2014). "A starch-binding domain identified in alpha-amylase (AmyP) represents a new family of carbohydrate-binding modules that contribute to enzymatic hydrolysis of soluble starch." FEBS Lett 588(7): 1161-1167.
  73. Piao, H., J. Froula, C. Du, T. W. Kim, E. R. Hawley, S. Bauer, Z. Wang, N. Ivanova, D. S. Clark, H. P. Klenk, et al. (2014). "Identification of novel biomass-degrading enzymes from genomic dark matter: Populating genomic sequence space with functional annotation." Biotechnol Bioeng 111(8): 1550-1565.
  74. Podar, M. and A. L. Reysenbach (2006). "New opportunities revealed by biotechnological explorations of extremophiles." Curr Opin Biotechnol 17(3): 250-255.
  75. Pope, P. B., A. K. Mackenzie, I. Gregor, W. Smith, M. A. Sundset, A. C. McHardy, M. Morrison and V. G. Eijsink (2012). "Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci." PLoS One 7(6): e38571.
  76. Prakash, O. and N. Jaiswal (2010). "alpha-Amylase: an ideal representative of thermostable enzymes." Appl Biochem Biotechnol 160(8): 2401-2414.
  77. Prasad, S., P. Manasa, S. Buddhi, P. Tirunagari, Z. Begum, S. Rajan and S. Shivaji (2014). "Diversity and bioprospective potential (cold-active enzymes) of cultivable marine bacteria from the subarctic glacial Fjord, Kongsfjorden." Curr Microbiol 68(2): 233-238.
  78. Radu, C. D., O. Parteni and L. Ochiuz (2016). "Applications of cyclodextrins in medical textiles - review." J Control Release 224: 146-157.
  79. Raghunathan, A., H. R. Ferguson, Jr., C. J. Bornarth, W. Song, M. Driscoll and R. S. Lasken (2005). "Genomic DNA amplification from a single bacterium." Appl Environ Microbiol 71(6): 3342- 3347.
  80. Rawlings, N. D. and F. R. Morton (2008). "The MEROPS batch BLAST: a tool to detect peptidases and their non-peptidase homologues in a genome." Biochimie 90(2): 243-259.
  81. Rinke, C., P. Schwientek, A. Sczyrba, N. N. Ivanova, I. J. Anderson, J. F. Cheng, A. Darling, S. Malfatti, B. K. Swan, E. A. Gies, et al. (2013). "Insights into the phylogeny and coding potential of microbial dark matter." Nature 499(7459): 431-437.
  82. Russell, R. J., U. Gerike, M. J. Danson, D. W. Hough and G. L. Taylor (1998). "Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium." Structure 6(3): 351-361.
  83. Schipper, C., C. Hornung, P. Bijtenhoorn, M. Quitschau, S. Grond and W. R. Streit (2009). "Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa." Appl Environ Microbiol 75(1): 224-233.
  84. Schloss, P. D. and J. Handelsman (2003). "Biotechnological prospects from metagenomics." Curr Opin Biotechnol 14(3): 303-310.
  85. Schmidt, T. M., E. F. DeLong and N. R. Pace (1991). "Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing." J Bacteriol 173(14): 4371-4378.
  86. Shendure, J., G. J. Porreca, N. B. Reppas, X. Lin, J. P. McCutcheon, A. M. Rosenbaum, M. D. Wang, K. Zhang, R. D. Mitra and G. M. Church (2005). "Accurate multiplex polony sequencing of an evolved bacterial genome." Science 309(5741): 1728-1732.
  87. Shinohara, M. L., M. Ihara, M. Abo, M. Hashida, S. Takagi and T. C. Beck (2001). "A novel thermostable branching enzyme from an extremely thermophilic bacterial species, Rhodothermus obamensis." Appl Microbiol Biotechnol 57(5-6): 653-659.
  88. Shiosaka, M. (1976). Heat stable cyclodextrin glycosyltransferase. Incorporated Hayashibara Biochemical Laboratories, Google Patents, US3988206 A Sievert, S. M. and C. Vetriani (2012). "Chemoautotrophy at Deep-Sea Vents Past, Present, and Future." Oceanography 25(1): 218-233.
  89. Simon, C. and R. Daniel (2011). "Metagenomic analyses: past and future trends." Appl Environ Microbiol 77(4): 1153-1161.
  90. Simon, C., J. Herath, S. Rockstroh and R. Daniel (2009). "Rapid identification of genes encoding DNA polymerases by function-based screening of metagenomic libraries derived from glacial ice." Appl Environ Microbiol 75(9): 2964-2968.
  91. Singh, B. K. (2010). "Exploring microbial diversity for biotechnology: the way forward." Trends Biotechnol 28(3): 111-116.
  92. Smith, S. P. and E. A. Bayer (2013). "Insights into cellulosome assembly and dynamics: from dissection to reconstruction of the supramolecular enzyme complex." Curr Opin Struct Biol 23(5): 686-694.
  93. Takai, K., S. Nakagawa, A. L. Reysenbach and J. Hoek (2006). Microbial Ecology of Mid-Ocean Ridges and Bac-Arc Basins. In Back-Arc Spreading Systems: Geological, Biological, Chemical, and Physical Interactions. Edited by Charles R. Fisher David M. Christie, Sang-Mook Lee andSharon Givens. American Geophysical Union. Geophysical Monograph Series. pp. 185-213.
  94. Takai, K. and K. Nakamura (2011). "Archaeal diversity and community development in deep-sea hydrothermal vents." Current Opinion in Microbiology 14(3): 282-291.
  95. Tamuri, M., M. Kanno and Y. Ishii (1981). Heat and acid-stable alpha-amylase enzymes and processes for producing the same. Cpc International Inc., Google Patents, US4284722 A Tasse, L., J. Bercovici, S. Pizzut-Serin, P. Robe, J. Tap, C. Klopp, B. L. Cantarel, P. M. Coutinho, B. Henrissat, M. Leclerc, et al. (2010). "Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes." Genome Res 20(11): 1605-1612.
  96. Teather, R. M. and P. J. Wood (1982). "Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen." Appl Environ Microbiol 43(4): 777-780.
  97. Thornburg, C. C., T. M. Zabriskie and K. L. McPhail (2010). "Deep-sea hydrothermal vents: potential hot spots for natural products discovery?" J Nat Prod 73(3): 489-499.
  98. Tivey, M. K. (2007). "Generation of seafloor hydrothermal vent fluids and associated mineral deposits." Oceanography 20(1): 50-65.
  99. Torsvik, V. and L. Ovreas (2002). "Microbial diversity and function in soil: from genes to ecosystems." Curr Opin Microbiol 5(3): 240-245.
  100. Trincone, A. (2011). "Marine biocatalysts: enzymatic features and applications." Mar Drugs 9(4): 478-499.
  101. Tyler, P. A., C. R. German, E. Ramirez-Llodra and C. L. Van Dover (2002). "Understanding the biogeography of chemosynthetic ecosystems." Oceanologica Acta 25(5): 227-241.
  102. Tyson, G. W., J. Chapman, P. Hugenholtz, E. E. Allen, R. J. Ram, P. M. Richardson, V. V. Solovyev, E. M. Rubin, D. S. Rokhsar and J. F. Banfield (2004). "Community structure and metabolism through reconstruction of microbial genomes from the environment." Nature 428(6978): 37-43.
  103. Uchiyama, T., T. Abe, T. Ikemura and K. Watanabe (2005). "Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes." Nat Biotechnol 23(1): 88-93.
  104. Uchiyama, T. and K. Miyazaki (2009). "Functional metagenomics for enzyme discovery: challenges to efficient screening." Curr Opin Biotechnol 20(6): 616-622.
  105. Uchiyama, T. and K. Miyazaki (2010). "Product-induced gene expression, a product-responsive reporter assay used to screen metagenomic libraries for enzyme-encoding genes." Appl Environ Microbiol 76(21): 7029-7035.
  106. Ufarte, L., E. Laville, S. Duquesne and G. Potocki-Veronese (2015a). "Metagenomics for the discovery of pollutant degrading enzymes." Biotechnol Adv 33(8): 1845-1854.
  107. van der Maarel, M. J., B. van der Veen, J. C. Uitdehaag, H. Leemhuis and L. Dijkhuizen (2002). "Properties and applications of starch-converting enzymes of the alpha-amylase family." J Biotechnol 94(2): 137-155.
  108. Vidal-Melgosa, S., H. L. Pedersen, J. Schuckel, G. Arnal, C. Dumon, D. B. Amby, R. N. Monrad, B. Westereng and W. G. Willats (2015). "A new versatile microarray-based method for high throughput screening of carbohydrate-active enzymes." J Biol Chem 290(14): 9020-9036.
  109. Vieille, C. and G. J. Zeikus (2001). "Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability." Microbiol Mol Biol Rev 65(1): 1-43.
  110. von Mering, C., P. Hugenholtz, J. Raes, S. G. Tringe, T. Doerks, L. J. Jensen, N. Ward and P. Bork (2007). "Quantitative phylogenetic assessment of microbial communities in diverse environments." Science 315(5815): 1126-1130.
  111. Xu, J., M. K. Bjursell, J. Himrod, S. Deng, L. K. Carmichael, H. C. Chiang, L. V. Hooper and J. I. Gordon (2003). "A genomic view of the human-Bacteroides thetaiotaomicron symbiosis." Science 299(5615): 2074-2076.
  112. Xu, J., F. Ren, C. H. Huang, Y. Zheng, J. Zhen, H. Sun, T. P. Ko, M. He, C. C. Chen, H. C. Chan, et al. (2014). "Functional and structural studies of pullulanase from Anoxybacillus sp. LM18- 11." Proteins 82(9): 1685-1693.
  113. Yan, X., A. Geng, J. Zhang, Y. Wei, L. Zhang, C. Qian, Q. Wang, S. Wang and Z. Zhou (2013). "Discovery of (hemi-) cellulase genes in a metagenomic library from a biogas digester using 454 pyrosequencing." Appl Microbiol Biotechnol 97(18): 8173-8182.
  114. Yang, X., J. H. Lee, H. Y. Yoo, H. Y. Shin, L. P. Thapa, C. Park and S. W. Kim (2014). "Production of bioethanol and biodiesel using instant noodle waste." Bioprocess Biosyst Eng 37(8): 1627-1635.
  115. Zeigler, D. R. (2001). The Genus Geobacillus -Introduction and Strain Catalog. Bacillus Genetic Stock Center -Catalog of Strains, 7th Edition, Volume 3. Department of Biochemistry Ohio State University, The Bacillus Genetic Stock Center.
  116. Zeikus, J. G. and H. H. Hyun (1987). Thermostable beta-amylase. Michigan Biotechnology Institute, Google Patents, US4647538 A Zhou, J., M. A. Bruns and J. M. Tiedje (1996). "DNA recovery from soils of diverse composition." Appl Environ Microbiol 62(2): 316-322.

Cited by

Sorted by citations

Authors
Stokke, R., Dahle, H., Roalkvam, I., Wissuwa, J., Daae, F. L., Tooming‐Klunderud, A., Thorseth, I. H., Pedersen, R. B., & Steen, I. H.
Affiliations
  • University of Bergen (NO)
  • University of Oslo (NO)
Corresponding author
Stokke, Runar
Venue
Environmental Microbiology
Publisher
Wiley
Published
2015-08-17
Volume
17
Issue
10
Pages
4063-4077
ISSN
  • 1462-2912 (ISSN-L)
  • 1462-2920
OpenAlex
W2152925133
Cited by
63
References
83
Citations by year
2025: 5 · 2024: 3 · 2023: 8 · 2022: 7 · 2021: 11 · 2020: 6 · 2019: 4 · 2018: 7 · 2017: 4 · 2016: 6 · 2015: 2
FWCI
5.74
Type
journal article
Language
en
Open access
Locations
  • Environmental Microbiology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Norwegian Research Council (208491, 221568, 179560)
  • ARGUS Remote Systems
Topics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
Keywords
Epsilonproteobacteria, Bacteroidetes, Sulfurovum, black smoker chimneys, microbial filaments, organotrophic bacteria, bacterial interactions, acetyl-CoA synthetase, acetate assimilation, organic matter recycling, deep-sea food webs
MeSH terms
Acetates, Acetyl Coenzyme A, Coenzyme A Ligases, Phylogeny, RNA, Ribosomal, 16S, Biofilms, Epsilonproteobacteria, Bacteroidetes, Microbial Interactions, Hydrothermal Vents

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review