Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Berg, Carlo ^a,c   Listmann, Luisa ^a   Vandieken, Verona ^a,b   Vogts, Angela ^a   Jürgens, Klaus ^a  

^a LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH   (Germany)

^b UNIVERSITY OF OLDENBURG   (Germany)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Ammonia oxidizing archaea; Baltic sea; Chemoautotrophy; CO2 fixation; Enrichment; Thaumarchaeota

Indexed keywords

AMMONIA; AMMONIUM CHLORIDE; BICARBONATE; RNA 16S;

AMMONIA MONOOXYGENASE SUBUNIT A; AMMONIA MONOOXYGENASE SUBUNIT A GENE; AMMONIA OXIDIZING ARCHAEON; ARTICLE; BACTERIAL GENE; BALTIC SEA; BIOMASS PRODUCTION; CARBON DIOXIDE FIXATION; CELL DENSITY; CELL FUNCTION; CELLULAR UPTAKE; CHEMOAUTOTROPHY; CONTROLLED STUDY; DNA EXTRACTION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE SEQUENCE; MICROBIAL GROWTH; NITROSOARCHAEUM; NONHUMAN; OXIDATION; PELAGIC ZONE; PHYLOGENY; SALINITY; THAUMARCHAEOTA;

ARCHAEA; LIMNIA;

EID: 84920653214     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00786     Document Type: Article

References (70)

1. Alonso-Sáez, L., Waller, A. S., Mende, D. R., Bakker, K., Farnelid, H., Yager, P. L., Lovejoy, C., Tremblay, J.-é., Potvin, M., Heinrich, F., Estrada, M., Riemann, L., Bork, P., Pedrós-Alió, C., and Bertilsson, S. (2012). Role for urea in nitrification by polar marine Archaea. Proc. Natl. Acad. Sci. U. S. A. 109, 17989-17994. doi:10.1073/pnas.1201914109.
2. Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R., and Stahl, D. A. (1990). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919-1925.
3. Beman, J. M., Popp, B. N., and Francis, C. A. (2008). Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2, 429-441. doi:10.1038/ismej.2007.118.
4. Berg, C., Vandieken, V., Thamdrup, B., and Jürgens, K. (in press). Significance of archaeal nitrification in hypoxic waters of the Baltic Sea. ISME J. doi: 10.1038/ismej.2014.218
5. Berg, I. A., Kockelkorn, D., Buckel, W., and Fuchs, G. (2007). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782-1786. doi:10.1126/science.1149976.
6. Biller, S. J., Mosier, A. C., Wells, G. F., and Francis, C. A. (2012). Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat. Front. Microbiol. 3, 252. doi:10.3389/fmicb.2012.00252.
7. Blainey, P. C., Mosier, A. C., Potanina, A., Francis, C. A., and Quake, S. R. (2011). Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6, e16626. doi:10.1371/journal.pone.0016626.
8. Bouskill, N. J., Eveillard, D., Chien, D., Jayakumar, A., and Ward, B. B. (2012). Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environ. M icrobiol. 14, 714-729. doi:10.1111/j.1462-2920.2011.02623.x.
9. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. (2008). Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252. doi:10.1038/nrmicro1852.
10. Caffrey, J. M., Bano, N., Kalanetra, K., and Hollibaugh, J. T. (2007). Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1, 660-662. doi:10.1038/ismej.2007.79.
11. Chain, P., Lamerdin, J., Larimer, F., Regala, W., Lao, V., Land, M., Hauser, L., Hooper, A., Klotz, M., Norton, J., Sayavedra-Soto, L., Arciero, D., Hommes, N., Whittaker, M., and Arp, D. (2003). Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. Society 185, 2759-2773. doi:10.1128/JB.185.9.2759.
12. Daims, H., Brühl, A., Amann, R., Schleifer, K. H., and Wagner, M. (1999). The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434-444. doi:10.1016/S0723-2020(99)80053-8.
13. DeLong, E. F. (1992). Archaea in coastal marine environments. Proc. Natl. Acad. Sci. U. S. A. 89, 5685-5689. doi:10.1073/pnas.89.12.5685.
14. Erguder, T. H., Boon, N., Wittebolle, L., Marzorati, M., and Verstraete, W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol. Rev. 33, 855-869. doi:10.1111/j.1574-6976.2009.00179.x.
15. Francis, C. A., Beman, J. M., and Kuypers, M. M. M. (2007). New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19-27. doi:10.1038/ismej.2007.8.
16. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., and Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U. S. A. 102, 14683-14688. doi:10.1073/pnas.0506625102.
17. French, E., Kozlowski, J. A., Mukherjee, M., Bullerjahn, G., and Bollmann, A. (2012). Enrichment and characterization of three ammonia-oxidizing Archaea from freshwater environments. Appl. Environ. Microbiol. 78, 5773-5780. doi:10.1128/AEM.00432-12.
18. Glaubitz, S., Kießlich, K., Meeske, C., Labrenz, M., and Jürgens, K. (2013). SUP05 dominates the gammaproteobacterial sulfur oxidizer assemblages in pelagic redoxclines of the central Baltic and Black Seas. Appl. Environ. Microbiol. 79, 2767-2776. doi:10.1128/AEM.03777-12.
19. Grasshoff, K., Ehrhardt, M., and Kremling, K. (1983). Methods of seawater analysis. Weinheim: Verlag Chemie (VCH).
20. Grote, J., Jost, G., Labrenz, M., Herndl, G. J., and Jürgens, K. (2008). Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in s ulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl. Environ. Microbiol. 74, 7546-7551. doi:10.1128/AEM.01186-08.
21. Grote, J., Schott, T., Bruckner, C. G., Glöckner, F. O., Jost, G., Teeling, H., Labrenz, M., and Jürgens, K. (2012). Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. Proc. Natl. Acad. Sci. U. S. A. 109, 506-510. doi:10.1073/pnas.1111262109.
22. Hallam, S. J., Konstantinidis, K. T., Putnam, N., Schleper, C., Watanabe, Y., Sugahara, J., Preston, C., de la Torre, J., Richardson, P. M., and DeLong, E. F. (2006a). Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. U. S. A. 103, 18296-18301. doi:10.1073/pnas.0608549103.
23. Hallam, S. J., Mincer, T. J., Schleper, C., Preston, C. M., Roberts, K., Richardson, P. M., and DeLong, E. F. (2006b). Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95. doi:10.1371/journal.pbio.0040095.
24. Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 4.
25. Hatzenpichler, R. (2012). Diversity, physiology and niche differentiation of ammonia-oxidizing archaea. Appl. Environ. Microbiol. 78, 7501-7510. doi:10.1128/AEM.01960-12.
26. Hatzenpichler, R., Lebedeva, E. V, Spieck, E., Stoecker, K., Richter, A., Daims, H., and Wagner, M. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. U. S. A. 105, 2134-2139. doi:10.1073/pnas.0708857105.
27. Herndl, G. J., Reinthaler, T., Teira, E., Aken, H. Van, Veth, C., Pernthaler, A., and Pernthaler, J. (2005). Contribution of archaea to total prokaryotic production in the deep atlantic ocean. Appl. Environ. Microbiol. 71, 2303-2309. doi:10.1128/AEM.71.5.2303.
28. Jansson, B. P., Malandrin, L., and Johansson, H. E. (2000). Cell cycle arrest in archaea by the hypusination inhibitor N1-guanyl-1,7-diaminoheptane. J. Bacteriol. 182, 1158-1161. doi:10.1128/JB.182.4.1158-1161.2000.
29. Jung, M.-Y., Park, S.-J., Min, D., Kim, J.-S., Rijpstra, W. I. C., Sinninghe Damsté, J. S., Kim, G.-J., Madsen, E. L., and Rhee, S.-K. (2011). Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl. Environ. Microbiol. 77, 8635-8647. doi:10.1128/AEM.05787-11.
30. Karner, M. B., DeLong, E. F., and Karl, D. M. (2001). Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507-510. doi:10.1038/35054051.
31. Klotz, M. G., Arp, D. J., Chain, P. S. G., El-Sheikh, A. F., Hauser, L. J., Hommes, N. G., Larimer, F. W., Malfatti, S. A., Norton, J. M., Poret-Peterson, A. T., Vergez, L.M. and Ward, B. (2006). Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol. 72, 6299-315. doi:10.1128/AEM.00463-06.
32. Könneke, M., Bernhard, A. E., de la Torre, J. R., Walker, C. B., Waterbury, J. B., and Stahl, D. A. (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543-546. doi:10.1038/nature03911.
33. Könneke, M., Schubert, D. M., Brown, P. C., Hügler, M., Standfest, S., Schwander, T., Schada Von Borzyskowski, L., Erb, T. J., Stahl, D. A., and Berg, I. A. (2014). Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc. Natl. Acad. Sci. U. S. A. 111, 8239-8244. doi:10.1073/pnas.1402028111.
34. Labrenz, M., Jost, G., and Jürgens, K. (2007). Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic-anoxic interface. Aquat. Microb. Ecol. 46, 177-190. doi:10.3354/ame046177.
35. Labrenz, M., Sintes, E., Toetzke, F., Zumsteg, A., Herndl, G. J., Seidler, M., and Jürgens, K. (2010). Relevance of a crenarchaeotal subcluster related to Candidatus Nitrosopumilus maritimus to ammonia oxidation in the suboxic zone of the central Baltic Sea. ISME J. 4, 1496-1508. doi:10.1038/ismej.2010.78.
36. Lam, P., Lavik, G., Jensen, M. M., van de Vossenberg, J., Schmid, M., Woebken, D., Gutiérrez, D., Amann, R., Jetten, M. S. M., and Kuypers, M. M. M. (2009). Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl. Acad. Sci. U. S. A. 106, 4752-4757. doi:10.1073/pnas.0812444106.
37. Lane, D. J. (1991). "16S/23S rRNA sequencing," in Nucleic acid techniques in bacterial systematics (Wiley), 125-175.
38. Lebedeva, E. V., Hatzenpichler, R., Pelletier, E., Schuster, N., Hauzmayer, S., Bulaev, A., Grigor'eva, N. V., Galushko, A., Schmid, M., Palatinszky, M., Le Paslier, D., Daims, H. and Wagner, M. (2013). Enrichment and genome sequence of the group I.1a ammonia-oxidizing archaeon "Ca. Nitrosotenuis uzonensis" representing a clade globally distributed in thermal habitats. PLoS One 8, e80835. doi:10.1371/journal.pone.0080835.
39. Lee, S., Fuhrman, J. A. (1987). Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 53 (6), 1298-1303.
40. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lüßmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., and Schleifer, K.-H. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi:10.1093/nar/gkh293.
41. Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R., Stahl, D. A., and Torre, R. De (2009). Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976-979. doi:10.1038/nature08465.
42. Matsutani, N., Nakagawa, T., Nakamura, K., Takahashi, R., Yoshihara, K., and Tokuyama, T. (2011). Enrichment of a novel marine ammonia-oxidizing archaeon obtained from sand of an eelgrass zone. Microbes Environ. 26, 23-29. doi:10.1264/jsme2.ME10156.
43. Middelburg, J. J. (2011). Chemoautotrophy in the ocean. Geophys. Res. Lett. 38, 94-97. doi:10.1029/2011GL049725.
44. Mosier, A. C., Lund, M. B., and Francis, C. A. (2012). Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb. Ecol. 64, 955-963. doi:10.1007/s00248-012-0075-1.
45. Musat, N., Foster, R., Vagner, T., Adam, B., and Kuypers, M. M. M. (2011). Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol. Rev., 486-511. doi:10.1111/j.1574-6976.2011.00303.x.
46. Mußmann, M., Brito, I., Pitcher, A., Sinninghe Damste, J. S., Hatzenpichler, R., Richter, A., Nielsen, J. L., Nielsen, P. H., Muller, A., Daims, H., Wagner, M. and Head, I. M. (2011). Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl. Acad. Sci. U. S. A., 108, 16771-16776. doi:10.1073/pnas.1106427108.
47. Nier, A. O. (1950). A redetermination of the relative abundances of the isotopes of carbon, nitrogen, oxygen, argon and potassium. Phys. Rev. Lett. 77, 789-793. doi:10.1103/PhysRev.77.789.
48. Ouverney, C. C., Fuhrman, J. A. (2000). Marine planktonic archaea take up amino acids. Applied and Environmental Microbiology, 66, 4829-4833. doi: 10.1128/AEM.66.11.4829-4833.2000
49. Pernthaler, A., Pernthaler, J., and Amann, R. (2002). Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094-3101. doi:10.1128/AEM.68.6.3094.
50. Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Overmann, J., Reinhold-Hurek, B., Loy, A., and Wagner, M. (2012). amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 14, 525-539. doi:10.1111/j.1462-2920.2011.02666.x.
51. Polerecky, L., Adam, B., Milucka, J., Musat, N., Vagner, T., and Kuypers, M. M. M. (2012). Look at NanoSIMS-a tool for the analysis of nanoSIMS data in environmental microbiology. Environ. Microbiol. 14, 1009-1023. doi:10.1111/j.1462-2920.2011.02681.x.
52. Pruesse, E., Peplies, J., and Glöckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823-1829. doi:10.1093/bioinformatics/bts252.
53. Purkhold, U., Pommerening-Röser, A., Juretschko, S., Schmid, M. C., Koops, H. P., Wagner, M. (2000). Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66, 5368-5382. doi:10.1128/AEM.66.12.5368-5382.2000.
54. Qin, W., Amin, S. A., Martens-Habbena, W., Walker, C. B., Urakawa, H., Devol, A. H., Ingalls, A. E., Moffett, J. W., Armbrust, E. V., and Stahl, D. A. (2014). Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc. Natl. Acad. Sci. U. S. A., 111, 12504-12509. doi:10.1073/pnas.1324115111.
55. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web based tools. Nucleic Acids Res. 41, D590-6. doi:10.1093/nar/gks1219.
56. Santoro, A. E., and Casciotti, K. L. (2011). Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J. 5, 1796-1808. doi:10.1038/ismej.2011.58.
57. Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D. A, Wagner, M., and Schleper, C. (2010). Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331-340. doi:10.1016/j.tim.2010.06.003.
58. Spang, A., Poehlein, A., Offre, P., Zumbrägel, S., Haider, S., Rychlik, N., Nowka, B., Schmeisser, C., Lebedeva, E. V., Rattei, T., Böhm, C., Schmid, M., Galushko, A., Hatzenpichler, R., Weinmaier, T., Daniel, R., Schleper, C., Spieck, E., Streit, W. and Wagner, M. (2012). The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14, 3122-3145. doi:10.1111/j.1462-2920.2012.02893.x.
59. Stahl, D., A. and Amann, R. (1991). "Development and application of nucleic acid probes in bacterial systematics," in Nucleic Acid Techniques in Bacterial Systematics., ed. M. Stackebrandt, E., Goodfellow (John Wiley and Sons, Chichester, UK), 205-248.
60. Stieglmeier, M., Klingl, A., Alves, R. J. E., Rittmann, S. K.-M. R., Melcher, M., Leisch, N., and Schleper, C. (2014). Nitrososphaera viennensis sp. nov., an aerobic and mesophilic ammonia oxidizing archaeon from soil and member of the archaeal phylum Thaumarchaeota. Int. J. Syst. Evol. Microbiol. 007536, 2738-2752. doi:10.1099/ijs.0.063172-0.
61. Teira, E., Burg, D., Aken, H. Van, Veth, C., and Herndl, G. J. (2006). Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol. Oceanogr. 51, 60-69.
62. Tijhuis, L., Van Loosdrecht, M. C., and Heijnen, J. J. (1993). A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol. Bioeng. 42, 509-519. doi:10.1002/bit.260420415.
63. Tourna, M., Stieglmeier, M., Spang, A., Könneke, M., Schintlmeister, A., and Urich, T. (2011). Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. U. S. A. 108, 8420-8425. doi:10.1073/pnas.1013488108.
64. Treusch, A. H., Leininger, S., Kletzin, A., Schuster, S. C., Klenk, H.-P., and Schleper, C. (2005). Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ. Microbiol. 7, 1985-1995. doi:10.1111/j.1462-2920.2005.00906.x.
65. Varela, M. M., van Aken, H. M., Sintes, E., Reinthaler, T., and Herndl, G. J. (2011). Contribution of Crenarchaeota and Bacteria to autotrophy in the North Atlantic interior. Environ. Microbiol. 13, 1524-33. doi:10.1111/j.1462-2920.2011.02457.x.
66. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D., Paulsen, I., Nelson, K. E., Nelson, W., Fouts, D.E., Levy, S., Knap, A.H., Lomas, M.W., Nealson, K., White, O., Peterson, J., Hoffman, J., Parsons, R., Baden-Tillson, H., Pfannkoch, C., Rogers, Y.-H. and Smith, H.O. (2004). Environmental Genome Shotgun Sequencing of the Sargasso Sea. Science 304, 66-74. doi:10.1126/science.1093857.
67. Walker, C. B., de la Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., Brochier-Armanet, C., Chain, P. S. G., Chan, P. P., Gollabgir, A., Hemp, J., Hügler, M., Karr, E.A., Könneke, M., Shin, M., Lawton, T.J., Lowe, T., Martens-Habbena, W., Sayavedra-Soto, L.A., Lang, D., Sievert, S.M., Rosenzweig, A.C., Manning, G. and Stahl, S. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U. S. A. 107, 8818-8123. doi:10.1073/pnas.0913533107.
68. Weinbauer, M. G., Fritz, I., Wenderoth, D. F., and Höfle, M. G. (2002). Simultaneous extraction from bacterioplankton of total RNA and DNA suitable for quantitative structure and function analyses. Appl. Environ. Microbiol. 68, 1082-1087. doi:10.1128/AEM.68.3.1082.
69. Wright, E. S., Yilmaz, L. S., and Noguera, D. R. (2012). DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78, 717-25. doi:10.1128/AEM.06516-11.
70. Wuchter, C., Abbas, B., Coolen, M. J. L., Herfort, L., van Bleijswijk, J., Timmers, P., Strous, M., Teira, E., Herndl, G. J., Middelburg, J. J., Schouten, S. and Sinninghe Damsté, J. (2006). Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U. S. A. 103, 12317-12322. doi:10.1073/pnas.0600756103.