Enhanced metabolic versatility of planktonic sulfur-oxidizing γ-proteobacteria in an oxygen-deficient coastal ecosystem

Frontiers in Marine Science

Volumn 1, Issue JUL, 2014, Pages

  Murillo, Alejandro A ^a   Ramírez Flandes, Salvador ^a,b   DeLong, Edward F ^c   Ulloa, Osvaldo ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

^b UNIVERSIDAD ADOLFO IBÁÑEZ   (Chile)

^c Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

ESP GSO; Metagenomic analysis; OMZ; Sulfur oxidizers; SUP05

Indexed keywords

EID: 85008949766     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2014.00018     Document Type: Article

References (58)

1. Anantharaman, K., Breier, J. A., Sheik, C. S., and Dick, G. J. (2013). Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 110, 330-335. doi: 10.1073/pnas.1215340110
2. Aravind, L., and Koonin, E. V. (2001). The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate-and iron-dependent dioxygenases. Genome Biol. 2, 0007.1-0007.8. doi: 10.1186/gb-2001-2-3-research0007
3. 2 acquisition by the CBB cycle. J. Exp. Bot. 59, 1525-1541. doi: 10.1093/jxb/erm297
4. Bano, N., and Hollibaugh, J. (2002). Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl. Environ. Microbiol. 68, 505-518. doi: 10.1128/AEM.68.2.505-518.2002
5. Berg, R. A., and Prockop, D. J. (1973). Affinity column purification of protocollagen proline hydroxylase from chick embryos and further characterization of the enzyme. J. Biol. Chem. 248, 1175-1182.
6. 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
7. Chen, B. J., Carroll, P., and Samson, L. (1994). The Escherichia coli AlkB protein protects human cells against alkylation-induced toxicity. J. Bacteriol. 176, 6255-6261.
8. Chiang, R. C., Cavicchioli, R., and Gunsalus, R. P. (1992). Identification and characterization of narQ, a second nitrate sensor for nitrate-dependent gene regulation in Escherichia coli. Mol. Microbiol. 6, 1913-1923. doi: 10.1111/j.1365-2958.1992.tb01364.x
9. Dahl, C., Engels, S., Pott-Sperling, A. S., Schulte, A., Sander, J., Lübbe, Y., et al. (2005). Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J. Bacteriol. 187, 1392-1404. doi: 10.1128/JB.187.4.1392-1404.2005
10. Darby, C., Cosma, C. L., Thomas, J. H., and Manoil, C. (1999). Lethal paralysis of Caenorhabditis elegans by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 96, 15202-15207. doi: 10.1073/pnas.96.26.15202
11. Dong, X. R., Li, S. F., and DeMoss, J. A. (1992). Upstream sequence elements required for NarL-mediated activation of transcription from the narGHJI promoter of Escherichia coli. J. Biol. Chem. 267, 14122-14128.
12. Drummond, A., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., et al. (2011). Geneious. Available online at: http://www.geneious.com/
13. Friedrich, C. G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001). Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl. Environ. Microbiol. 67, 2873-2882. doi: 10.1128/AEM.67.7.2873-2882.2001
14. Frigaard, N.-U., and Bryant, D. A. (2008). "Genomic and evolutionary perspectives on sulfur metabolism in green sulfur bacteria, " in Microbial Sulfur Metabolism, eds C. Dahl and C. G. Friedrich (New York, NY; Berlin; Heidelberg: Springer-Verlag), 60-73.
15. Fuchs, B. M., Woebken, D., Zubkov, M. V., Burkill, P., and Amann, R. (2005). Molecular identification of picoplankton populations in contrasting waters of the Arabian Sea. Aquat. Microb. Ecol. 39, 145-157. doi: 10.3354/ame039145
16. Galán, A., Molina, V., Belmar, L., and Ulloa, O. (2012). Temporal variability and phylogenetic characterization of planktonic anammox bacteria in the coastal upwelling ecosystem off central Chile. Prog. Oceanogr. 95, 110-120. doi: 10.1016/j.pocean.2011.07.007
17. Gennis, R. B., and Stewart, V. (1996). "Respiration, " in Escherchia coli and Salmonella: Cellular and Molecular Biology, eds F. C. Neidhardt, R. Curtis III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (Washington DC: ASM Press), 217-261.
18. Ghosh, W., and Dam, B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol. Rev. 33, 999-1043. doi: 10.1111/j.1574-6976.2009.00187.x
19. 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
20. Grimm, F., Franz, B., and Dahl, C. (2008). "Thiosulfate and sulfur oxidation in purple sulfur bacteria, microbial sulfur metabolism, " in Microbial Sulfur Metabolism, eds C. Dahl and C. G. Friedrich (New York, NY; Berlin; Heidelberg: Springer-Verlag), 101-116.
21. Hutton, J. J., Tappel, A. L., and Udenfriend, S. (1967). Cofactor and substrate requirements of collagen proline hydroxylase. Arch. Biochem. Biophys. 118, 231-240. doi: 10.1016/0003-9861(67)90302-5
22. Jensen, M. M., Lam, P., Revsbech, N. P., Nagel, B., Gaye, B., Jetten, M. S., et al. (2011). Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J. 5, 1660-1670. doi: 10.1038/ismej.2011.44
23. Jormakka, M., Byrne, B., and Iwata, S. (2003). Proton motive force generation by a redox loop mechanism. FEBS Lett. 545, 25-30. doi: 10.1016/S0014-5793(03)00389-2
24. Kivirikko, K. I., Kishida, Y., Sakakibara, S., and Prockop, J. (1972). Hydroxylation of (X-Pro-Gly)n by protocollagen proline hydroxylase. Effect of chain length, helical conformation and amino acid sequence in the substrate. Biochim. Biophys. Acta 271, 347-356. doi: 10.1016/0005-2795(72)90209-7
25. Kondo, H., Nakabeppu, Y., Kataoka, H., Kuhara, S., Kawabata, S., and Sekiguchi, M. (1986). Structure and expression of the alkB gene of Escherichia coli related to the repair of alkylated DNA. J. Biol. Chem. 261, 15772-15777.
26. Kuwahara, H., Yoshida, T., Takaki, Y., Shimamura, S., Nishi, S., Harada, M., et al. (2007). Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr. Biol. 17, 881-886. doi: 10.1016/j.cub.2007.04.039
27. Lam, P., Jensen, M. M., Lavik, G., McGinnis, D. F., Müller, B., Schubert, C. J., et al. (2007). Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. U.S.A. 104, 7104-7109. doi: 10.1073/pnas.0611081104
28. Lam, P., and Kuypers, M. M. M. (2011). Microbial nitrogen cycling processes in oxygen minimum zones. Ann. Rev. Mar. Sci. 3, 317-345. doi: 10.1146/annurev-marine-120709-142814
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, 581-584. doi: 10.1038/nature07588
30. Lin, J. T., and Stewart, V. (1998). Nitrate assimilation by bacteria. Adv. Microb. Physiol. 39, 1-30, 379.
31. Malm, S., Tiffert, Y., Micklinghoff, J., Schultze, S., Joost, I., Weber, I., et al. (2009). The roles of the nitrate reductase NarGHJI, the nitrite reductase NirBD and the response regulator GlnR in nitrate assimilation of Mycobacterium tuberculosis. Microbiology 155, 1332-1339. doi: 10.1099/mic.0.023275-0
32. Marshall, K. T., and Morris, R. M. (2013). Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J. 7, 452-455. doi: 10.1038/ismej.2012.78
33. Molina, V., Belmar, L., and Ulloa, O. (2010). High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygen-deficient waters of the eastern South Pacific. Environ. Microbiol. 12, 2450-2465. doi: 10.1111/j.1462-2920.2010.02218.x
34. Montero, P., Daneri, G., Cuevas, L. A., González, H. E., Jacob, B., Lizárraga, L., et al. (2007). Productivity cycles in the coastal upwelling area off Concepción: the importance of diatoms and bacterioplankton in the organic carbon flux. Prog. Oceanogr. 75, 518-530. doi: 10.1016/j.pocean.2007.08.013
35. Otte, S., Kuenen, J., Nielsen, L., Paerl, H., Zopfi, J., Schulz, H., et al. (1999). Nitrogen, carbon, and sulfur metabolism in natural thioploca samples. Appl. Environ. Microbiol. 65, 3148-3157.
36. Philippot, L. (2002). Denitrifying genes in bacterial and archaeal genomes. Biochim. Biophys. Acta 1577, 355-376. doi: 10.1016/S0167-4781(02)00420-7
37. Poretsky, R. S., Sun, S., Mou, X., and Moran, M. A. (2010). Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon. Environ. Microbiol. 12, 616-627. doi: 10.1111/j.1462-2920.2009.02102.x
38. Pott, A. S., and Dahl, C. (1998). Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144, 1881-1894. doi: 10.1099/00221287-144-7-1881
39. Revsbech, N., Larsen, L., Gundersen, J., Dalsgaard, T., Ulloa, O., and Thamdrup, B. (2009). Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol. Oceanogr. Methods 7, 371-381. doi: 10.4319/lom.2009.7.371
40. Roeselers, G., Newton, I. L. G., Woyke, T., Auchtung, T. A., Dilly, G. F., Dutton, R. J., et al. (2010). Complete genome sequence of Candidatus Ruthia magnifica. Stand. Genomic Sci. 3, 163-173. doi: 10.4056/sigs.1103048
41. Sánchez, O., Ferrera, I., Dahl, C., and Mas, J. (2001). In vivo role of adenosine-5'-phosphosulfate reductase in the purple sulfur bacterium Allochromatium vinosum. Arch. Microbiol. 176, 301-305. doi: 10.1007/s002030100327
42. Sander, J., Engels-Schwarzlose, S., and Dahl, C. (2006). Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch. Microbiol. 186, 357-366. doi: 10.1007/s00203-006-0156-y
43. Shao, M.-F., Zhang, T., and Fang, H. H.-P. (2010). Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl. Microbiol. Biotechnol. 88, 1027-1042. doi: 10.1007/s00253-010-2847-1
44. Sobarzo, M., Bravo, L., Donoso, D., Garcés-Vargas, J., and Schneider, W. (2007). Coastal upwelling and seasonal cycles that influence the water column over the continental shelf off central Chile. Prog. Oceanogr. 75, 363-382. doi: 10.1016/j.pocean.2007.08.022
45. Stevens, H., and Ulloa, O. (2008). Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ. Microbiol. 10, 1244-1259. doi: 10.1111/j.1462-2920.2007.01539.x
46. Stewart, F. J., Ulloa, O., and DeLong, E. F. (2012). Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ. Microbiol. 14, 23-40. doi: 10.1111/j.1462-2920.2010.02400.x
47. Stewart, V. (1988). Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol. Rev. 52, 190-232.
48. Sunamura, M., Higashi, Y., Miyako, C., Ishibashi, J., and Maruyama, A. (2004). Two bacteria phylotypes are predominant in the Suiyo Seamount hydrothermal plume. Appl. Environ. Microbiol. 70, 1190. doi: 10.1128/AEM.70.2.1190-1198.2004
49. Swan, B. K., Martinez-Garcia, M., Preston, C. M., Sczyrba, A., Woyke, T., Lamy, D., et al. (2011). Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296-1300. doi: 10.1126/science.1203690
50. Teske, A. (2010). Oceans. Cryptic links in the ocean. Science 330, 1326-1327. doi: 10.1126/science.1198400
51. Ulloa, O., Canfield, D. E., DeLong, E. F., Letelier, R. M., and Stewart, F. J. (2012). Microbial oceanography of anoxic oxygen minimum zones. Proc. Natl. Acad. Sci. U.S.A. 109, 15996-16003. doi: 10.1073/pnas.1205009109
52. Walker, M. S., and DeMoss, J. A. (1994). NarL-phosphate must bind to multiple upstream sites to activate transcription from the narG promoter of Escherichia coli. Mol. Microbiol. 14, 633-641. doi: 10.1111/j.1365-2958.1994.tb01302.x
53. 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
54. Wei, Y. F., Carter, K. C., Wang, R. P., and Shell, B. K. (1996). Molecular cloning and functional analysis of a human cDNA encoding an Escherichia coli AlkB homolog, a protein involved in DNA alkylation damage repair. Nucleic Acids Res. 24, 931-937. doi: 10.1093/nar/24.5.931
55. Wood, A. P., Aurikko, J. P., and Kelly, D. P. (2004). A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy? FEMS Microbiol. Rev. 28, 335-352. doi.: 10.1016/j.femsre.2003.12.001
56. Wright, J. J., Konwar, K. M., and Hallam, S. J. (2012). Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381-394. doi: 10.1038/nrmicro2778
57. Zhang, S., and Bryant, D. A. (2011). The tricarboxylic acid cycle in cyanobacteria. Science 334, 1551-1553. doi: 10.1126/science.1210858
58. Zhu, W., Lomsadze, A., and Borodovsky, M. (2010). Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132. doi: 10.1093/nar/gkq275