Recoding of the stop codon UGA to glycine by a BD1-5/SN-2 bacterium and niche partitioning between Alpha- and Gammaproteobacteria in a tidal sediment microbial community naturally selected in a laboratory chemostat

Frontiers in Microbiology

Volumn 5, Issue MAY, 2014, Pages

  Hanke, Anna ^a   Hamann, Emmo ^a   Sharma, Ritin ^b,c   Geelhoed, Jeanine S ^a   Hargesheimer, Theresa ^a   Kraft, Beate ^a   Meyer, Volker ^a   Lenk, Sabine ^a   Osmers, Harald ^a   Wu, Rong ^d   Makinwa, Kofi ^d   Hettich, Robert L ^b,c   Banfield, Jillian F ^e,f   Tegetmeyer, Halina E ^a,g   Strous, Marc ^a,g,h  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF TENNESSEE   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d Delft University of Technology ^*  (Netherlands)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g BIELEFELD UNIVERSITY   (Germany)

^h UNIVERSITY OF CALGARY   (Canada)

Author keywords

Chemostat; Continuous culture; Enrichment; Maritimibacter; Roseobacter; Stop codon

Indexed keywords

GLYCINE;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIUM; BD1 5/SN 2 BACTERIUM; COMPUTER MODEL; CONTINUOUS CULTURE; DENITRIFICATION; DNA SEQUENCE; ECOLOGICAL NICHE; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENE SEQUENCE; MASS SPECTROMETRY; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENETIC TREE; PHYLOGENY; PREDICTION; PROTEIN EXPRESSION; PROTEOMICS; SEDIMENT; SEQUENCE ALIGNMENT; SPECTROPHOTOMETRY; STOP CODON;

EID: 84904861504     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00231     Document Type: Article

References (60)

1. Albertsen, M., Hugenholtz, P., Skarshewski, A., Nielsen, K. L., Tyson, G. W., and Nielsen, P. H. (2013). Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-538. doi: 10.1038/nbt.2579
2. Amann, R., 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. Andrews, J. H., and Harris, R. F. (1986). r- and K-selection and microbial ecology. Adv. Microb. Ecol. 9, 99-147. doi: 10.1007/978-1-4757-0611-6_3
4. Baker, B. J., Comolli, L., Dick, G., Hauser, L., Hyatt, D., Dill, B. D., et al. (2010). Enigmatic, ultra-small uncultivated Archaea. Proc. Natl. Acad. Sci. U.S.A. 107, 8806-8811. doi: 10.1073/pnas.0914470107
5. Belnap, C. P., Pan, C., VerBerkmoes, N. C., Power, M. E., Samatova, N. F., Carver, R. L., et al. (2009). Cultivation and quantitative proteomic analyses of acidophilic microbial communities. ISME J. 4, 520-530. doi: 10.1038/ismej.2009.139
6. Bendschneider, K., and Robinson, R. J. (1952). A new spectrophotometric method for the determination of nitrite in sea water. J. Mar. Res. 11, 87-96.
7. Blainey, P. C. (2013). The future is now: single-cell genomics of bacteria and archaea. FEMS Microbiol. Rev. 37, 407-427. doi: 10.1111/1574-6976.12015
8. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi: 10.1186/1471-2105-10-421
9. Campbell, J. H., O'Donoghue, P., Campbell, A. G., Schwientek, P., Sczyrba, A., Woyke, T., et al. (2013). UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc. Natl. Acad. Sci. U.S.A. 110, 5540-5545. doi: 10.1073/pnas.1303090110
10. Canfield, D. E., Stewart, F. J., Thamdrup, B., De Brabandere, L., Dalsgaard, T., Delong, E. F., et al. (2010). A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330, 1375-1378. doi: 10.1126/science.1196889
11. Carpenter, L. J., Archer, S. D., and Beale, R. (2012). Ocean-atmosphere trace gas exchange. Chem. Soc. Rev. 41, 6473-6506. doi: 10.1039/c2cs35121h
12. Castelle, C. J., Hug, L. A., Wrighton, K. C., Thomas, B. C., Williams, K. H., Wu, D., et al. (2013). Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. Nat. Commun. 4, 2120. doi: 10.1038/ncomms3120
13. Clark, I. C., Melnyk, R. A., Engelbrektson, A., and Coates, J. D. (2013). Structure and evolution of chlorate reduction composite transposons. mBio 4, e00379-13. doi: 10.1128/mBio.00379-13
14. Coates, J. D., and Achenbach, L. A. (2004). Microbial perchlorate reduction: rocket-fuelled metabolism. Nat. Rev. Microbiol. 2, 569-580. doi: 10.1038/nrmicro926
15. Daims, H., Bruehl, 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
16. Dutilh, B. E., Jurgelenaite, R., Szklarczyk, R., van Hijum, S. A., Harhangi, H. R., Schmid, M., et al. (2011). FACIL: fast and accurate genetic code inference and logo. Bioinformatics 27, 1929-1933. doi: 10.1093/bioinformatics/btr316
17. Eddy, S. R. (2011). Accelerated profile HMM searches. PLoS Comput. Biol. 7:e1002195. doi: 10.1371/journal.pcbi.1002195
18. Eilers, H., Pernthaler, J., Peplies, J., Gloeckner, F. O., Gerdts, G., and Amann, R. (2001). Isolation of novel pelagic bacteria from the German bight and their seasonal contributions to surface picoplankton. Appl. Environ. Microbiol. 67, 5134-5142. doi: 10.1128/AEM.67.11.5134-5142.2001
19. Flood, B. E. (2010). The Utilization of Important Derivatives (TMA & Thiotaurine) of Eukaryotic Osmolytes by Novel Strains of Eubacteria. Available online at: //gradworks.umi.com/34/34/3434417.html. publication number 3434417.
20. Hyatt, D., Chen, G. L., Locascio, P. F., Land, M. L., Larimer, F. W., and Hauser, L. J. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. doi: 10.1186/1471-2105-11-119
21. Kalisky, T., and Quake, S. R. (2011). Single-cell genomics. Nat. Methods 8, 311-314. doi: 10.1038/nmeth0411-311
22. Kartal, B., and Strous, M. (2008). "Methods to study consortia and mixed cultures," in Accessing Uncultivated Microorganisms, ed K. Zengler (Washington, DC: ASM Press), 205-219.
23. Katoh, K., Misawa, K., Kuma, K. I., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res. 30, 3059-3066. doi: 10.1093/nar/gkf436
24. Kieskamp, W. M. L. L., Epping, W., and Helder, W. (1991). Seasonal variation in denitrification rates and nitrous oxide fluxes in intertidal sediments of the western Wadden Sea. Mar. Ecol. Prog. Ser. 72, 145-151. doi: 10.3354/meps072145
25. Kirchman, D. (2002). The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39, 91-100. doi: 10.1016/S0168-6496(01)00206-9
26. Kleiner, M., Wentrup, C., Lott, C., Teeling, H., Wetzel, S., Young, J., et al. (2012). Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proc. Natl. Acad. Sci. U.S.A. 109, E1173-E1182. doi: 10.1073/pnas.1121198109
27. Langmead, B., and Salzberg, S. L. (2012). Fast gapped-read alignment with bowtie 2. Nat. Methods 9, 357-359. doi: 10.1038/nmeth.1923
28. Laslett, D., and Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32, 11-16. doi: 10.1093/nar/gkh152
29. Lavik, G., Stührmann, T., Brüchert, V., Van der Plas, A., Mohrholz, V., Lam, P., et al. (2009). Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature 457, 581-585. doi: 10.1038/nature07588
30. Lee, K., Choo, Y. J. J., Giovannoni, S. J., and Cho, J. C. C. (2007). Maritimibacter alkaliphilus gen. nov., sp. nov., a genome-sequenced marine bacterium of the Roseobacter clade in the order Rhodobacterales. Int. J. Syst. Evol. Microbiol. 57, 1653-1658. doi: 10.1099/ijs.0.64960-0
31. Lenk, S., Arnds, J., Zerjatke, K., Musat, N., Amann, R., and Mußmann, M. (2011). Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environ. Microbiol. 13, 758-774. doi: 10.1111/j.1462-2920.2010.02380.x
32. Llobet-Brossa, E., Rosselló-Mora, R., and Amann, R. (1998). Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl. Environ. Microbiol. 64, 2691-2696.
33. Lo, I., Denef, V. J., VerBerkmoes, N. C., Shah, M. B., Goltsman, D., DiBartolo, G., et al. (2007). Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446, 537-541. doi: 10.1038/nature05624
34. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin-phenol reagent. J. Biol. Chem. 193, 265-275.
35. Ma, Z. Q., Dasari, S., Chambers, M. C., Litton, M. D., Sobecki, S. M., Zimmerman, L. J., et al. (2009). IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J. Proteome Res. 8, 3872-3881. doi: 10.1021/pr900360j
36. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K. H. (1992). Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria-problems and solutions. Syst. Appl. Microbiol. 15, 593-600. doi: 10.1016/S0723-2020(11)80121-9
37. McCutcheon, J. P., McDonald, B. R., and Moran, N. A. (2009). Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial Symbiont. PLoS Genet. 5:e1000565. doi: 10.1371/journal.pgen.1000565
38. Miller, C. S., Baker, B. J., Thomas, B. C., Singer, S. W., and Banfield, J. F. (2011). EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol. 12, R44. doi: 10.1186/gb-2011-12-5-r44
39. Narasingarao, P., and Häggblom, M. M. (2006). Sedimenticola selenatireducens, gen. nov., sp. nov., an anaerobic selenate-respiring bacterium isolated from estuarine sediment. Syst. Appl. Microbiol. 29, 382-388. doi: 10.1016/j.syapm.2005.12.011
40. Neef, A. (1997). PhD Thesis. Technische Universitaet Muenchen, Munich.
41. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2 - approximately Maximum-Likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490
42. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596. doi: 10.1093/nar/gks1219
43. Ramette, A. (2009). Quantitative community fingerprinting methods for estimating theabundance of operational taxonomic units in natural microbial communities. Appl. Environ. Microbiol. 75, 2495-2505. doi: 10.1128/AEM.02409-08
44. Rapid Library Preparation Method Manual. (2011). Available online at: http://454.com/downloads/my454/documentation/gs-flx-plus/Rapid-Library-Preparation-Method-Manual_XLPlus_May2011.pdf
45. Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J. F., et al. (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437. doi: 10.1038/nature12352
46. Solorzano, L. (1969). Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol. Oceanogr. 14, 799-801. doi: 10.4319/lo.1969.14.5.0799
47. Stewart, F. J. (2011). Dissimilatory sulfur cycling in oxygen minimum zones: an emerging metagenomics perspective. Biochem. Soc. Trans. 39, 1859-1863. doi: 10.1042/BST20110708
48. Strous, M., Kraft, B., Bisdorf, R., and Tegetmeyer, H. E. (2012). The binning of metagenomic contigs for microbial physiology of mixed cultures. Front. Microbiol. 3:410. doi: 10.3389/fmicb.2012.00410
49. Tabb, D. L., Fernando, C. G., and Chambers, M. C. (2007). MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661. doi: 10.1021/pr0604054
50. Thiele, S., Fuchs, B. M., and Amann, R. I. (2011). "Identification of microorganisms using the ribosomal RNA approach and fluorescence in situ hybridization," in Treatise on Water Science, Vol. 3, ed P. Wilderer (Oxford: Academic Press), 171-189.
51. Thrash, J. C., Cho, J. C., Ferriera, S., Johnson, J., Vergin, K. L., and Giovannoni, S. J. (2010). Genome sequences of Pelagibaca bermudensis HTCC2601T and Maritimibacter alkaliphilus HTCC2654T, the type strains of two marine Roseobacter genera. J. Bacteriol. 192, 5552-5553. doi: 10.1128/JB.00873-10
52. Tyson, G. W., Chapman, J., Hugenholtz, P., Allen, E. E., Ram, R. J., Richardson, P. M., et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37-43. doi: 10.1038/nature02340
53. Wallner, G., Amann, R., and Beisker, W. (1993). Optimizing fluorescent in situ hybridization with ribosomal-RNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136-143. doi: 10.1002/cyto.990140205
54. Walsh, D. A., Zaikova, E., Howes, C. G., Song, Y. C., Wright, J. J., Tringe, S. G., et al. (2009). Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326, 578-582. doi: 10.1126/science.1175309
55. Wisniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009). Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362. doi: 10.1038/nmeth.1322
56. Wrighton, K. C., Thomas, B. C., Sharon, I., Miller, C. S., Castelle, C. J., Ver Berkmoes, N. C., et al. (2012). Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661-1665. doi: 10.1126/science.1224041
57. Wu, R., Huijsing, J. H., and Makinwa, K. A. A. (2012). A 21b ±40mV range read-out IC for bridge transducers. J Solid-State Circ. 47, 2152-2163. doi: 10.1109/JSSC.2012.2197929
58. Würgler Hansen, J., Thamdrup, B., and Jørgensen, B. B. (2000). Anoxic incubation of sediment in gas-tight plastic bags: a method for biogeochemical process studies. Mar. Ecol. Prog. Ser. 208, 273-282. doi: 10.3354/meps208273
59. Yamao, F., Muto, A., Kawauchi, Y., Iwami, M., Iwagami, S., Azumi, Y., et al. (1985). UGA is read as tryptophan in Mycoplasma capricolum. Proc. Natl. Acad. Sci. U.S.A. 82, 2306-2309. doi: 10.1073/pnas.82.8.2306
60. Zhou, J., Bruns, M. A., and Tiedje, J. M. (1996). DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316-322.