Real-time PCR quantification and diversity analysis of the functional genes aprA and dsrA of sulfate-reducing prokaryotes in marine sediments of the Peru continental margin and the Black Sea

Frontiers in Microbiology

Volumn 2, Issue DEC, 2011, Pages

  Blazejak, Anna ^a,c   Schippers, Axel ^a,b  

^a FEDERAL INSTITUTE FOR GEOSCIENCES AND NATURAL RESOURCES BGR   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

Apra; Deep biosphere; Dsra; Odp; Real time PCR; Subsurface; Sulfate reducing prokaryotes

Indexed keywords

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 84875499456     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00253     Document Type: Article

References (68)

1. Agrawal, A., and Lal, B. (2009). Rapid detection and quantification of bisulfite reductase genes in oil field samples using real-time PCR. FEMS Microbiol. Ecol. 69, 301-312.
2. Bahr, M., Crump, B. C.,Klepac-Ceraj,V., Teske, A., Sogin, M. L., and Hobbie, J. E. (2005). Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. Environ. Microbiol. 7,1175-1185.
3. Ben-Dov, E., Brenner, A., and Kush-maro, A. (2007). Quantification of sulfate-reducing bacteria in industrial wastewater, by real-time poly-merase chain reaction (PCR) using dsr A and apsA genes. Microbiol Ecol. 54,439-451.
4. Blazejak, A., Erseus, C., Amann, R., and Dubilier, N. (2005). Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71, 1553-1561.
5. Blazejak, A., and Schippers, A. (2010). High abundance of JS-1- and Chlo-roflexi-related Bacteria in deeply buried marine sediments revealed by quantitative, real-time PCR. FEMS Microbiol. Ecol. 72, 198-207.
6. Böning, P., Brumsack, H.-L, Bottcher, M. E., Schnetger, B., Kriete, C., Kallmeyer, J., and Borchers, S. L. (2004). Geochemistry of Peruvian near-surface sediments. Geochim Cosmo chim Acta 68, 4429-4451.
7. Bottrell, S. H., Böttcher, M. E., Schippers, A., Parkes, R. J., Jørgensen, B. B, Raiswell, R., Telling, J., and Gehre, M. (2008). Abiotic sulfide oxidation via manganese fuels the deep biosphere. GoldschmidtConference Abstracts. Geochim. Cos-mochim. Acta 72(Suppl. 1), A102.
8. Bottrell, S. H., Parkes, R. J., Cragg, B. A., and Raiswell, R. (2000). Iso-topic evidence for anoxic pyrite oxidation and stimulation of bacterial sulphate reduction in marine sediments. J. Geol. Soc. London 157, 711-714.
9. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., andWittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments. Clin. Chem. 55,611-622.
10. Castresana, J., and Moreira, D. (1999). Respiratory chains in the last common ancestor of living organisms. J. Mol. Evol. 49,453-460.
11. Dhillon, A., Teske, A., Dillon, J., Stahl, D. A., and Sogin, M. L. (2003). Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Appl. Environ. Microbiol. 69, 2765-2772.
12. D'Hondt, S. L., Jørgensen, B. B., Miller, D. J., Batzke, A., Blake, R., Cragg, B. A., Cypionka, H., Dickens, G. R., Ferdelman, T. G., Hinrichs, K. U., Holm, N. G., Mitterer, R., Spivack, A., Wang, G., Bekins, B., Engelen, B., Ford, K., Gettemy, G., Rutherford, S. D., Sass, H., Skilbeck, C. G., Aiello, I. W., Guèrin, G., House, C. H., Inagaki, E, Meister, P., Naehr, T., Niitsuma, S., Parkes, R. J., Schippers, A., Smith, D. C., Teske, A., Wiegel, J., Padilla, C. N., and Solis Acosta, J. L. (2004). Distributions of microbial activities in deep subseafloor sediments. Science 306,2216-2221.
13. D'Hondt, S. L, Jørgensen, B, B., Miller, D. J., and Shipboard Scientific Party. (2003). Leg 201 Initial report - controls on microbial communities in deeply buried sediments, Eastern Equatorial Pacific and Peru margin. Proc. ODP, Init. Repts., 201: College Station, TX (Ocean 131 Drilling Program). doi: 10.2973/odp.proc.ir.201.2003.
14. Engelen, B., Ziegelmüller, K., Wolf, L., Köpke, B., Gittel, A., Cypionka, H., Treude, T., Nakagawa, S., Inagaki, F., Lever, M. A., and Steinsbu, B. O. (2008). Fluids from the oceanic crust support microbial activities within the deep biosphere. Geomicrobiol. J. 25, 56-66.
15. Ferdelman, T. G., Lee, C., Pantoja, S., Harder, J., Bebout, B. M., and Fos-sing, H. (1997). Sulfate reduction and methanogenesis in a Thioploca-dominated sediment off the coast of Chile. Geochim. Cosmochim. Acta 61, 3065-3079.
16. Friedrich, M. W (2002). Phylogenetic analysis reveals multiple lateral transfers of adenosine-5'-phos-phosulfate reductase genes among sulfate-reducing microorganisms. J. Bacteriol. 184,278-289.
17. Fry, J. C., Parkes, J. R., Cragg, B. A., Weightman, A. J., and Webster, G. (2008). Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiol. Ecol. 66, 181-196.
18. Geets, J., Borremans, B., Diels, L., Springael, D., Vangronsveld, J., van der Lelie, D., and Vanbroekhoven, K. (2006). DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J. Microbiol. Methods 66, 194-205.
19. Gittel, A., Mußmann, M., Sass, H., Cypionka, H., and Könneke, M. (2008). Identity and abundance of active sulfate-reducing bacteria in deep tidal flat sediments determined by directed cultivation and CARD-FISH analysis. Environ. Microbiol. 10,2645-2658.
20. Hartzell, P., and Reed, D. W (2006). The genus Archaeoglobus. Prokaryotes 3, 82-100.
21. Holmkvist, L., Kamyshny, A. Jr., Vogt, C., Vamvakopoulos, K., Ferdelman, T. G., and Jørgensen, B. B. (2011a). Sulfate reduction below the sulfate- methane transition in Black Sea sediments. Deep Sea Res. PartI Oceanogr. Res. Pap. 58, 493-504.
22. Holmkvist, L., Ferdelman, T. G., and Jørgensen, B. B. (2011b). A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark). Geochim. Cosmochim. Acta 75, 3581-3599.
23. Imachi, H., Sekiguchi, Y., Kamagata, Y., Loy, A., Qiu, Y. L., Hugenholtz, P., Kimura, N., Wagner, M., Ohashi, A., andHarada,H. (2006). Non-sulfate-reducing, syntrophic bacteria affiliated with Desulfotomaculum cluster I are widely distributed in methanogenic environments. Appl. Environ. Microbiol. 72, 2080-2091.
24. Inagaki, F., Nunoura, T., Nakagawa, S., Teske, A., Lever, M., Lauer, A., Suzuki, M., Takai, K., Delwiche, M., Col-well, F. S., Nealson, K. H., Horikoshi, K., D'Hondt, S., and Jørgensen, B. B. (2006). Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific ocean margin. Proc. Natl. Acad. Sci. U.S.A. 103,2815-2820.
25. Inagaki, F., Okada, H., Tsapin, A. I., and Nealson, K. H. (2005). The pale-ome: a sedimentary genetic record of past microbial communities. Astro-biology 5, 141-153.
26. Jørgensen, B. B. (1982). Mineralization of organic matter in the sea bed; the role of sulphate reduction. Nature 296, 643-645.
27. Jørgensen, B. B., D'Hondt, S., and Miller, D. J. (eds). (2005). Proc. ODP, Sci. Results, 201. Available at: http:// www-odp.tamu.edu/publications/ 20 1_SR/synth/synth.htm
28. Jørgensen, B. B., Weber, A., and Zopfi, J. (2001). Sulfate reduction and anaerobic methane oxidation in Black Sea sediments. Deep Sea Res. Part 1 Oceanogr. Res. Pap. 48, 2097-2120.
29. Julies, E. M., Fuchs, B. M., Arnosti, C., and Brüchert, V. (2010). Organic carbon degradation in anoxic organic-rich shelf sediments: bio-geochemical rates and microbial abundance. Geomicrobiol J. 27, 303-314.
30. Kaneko, R., Hayashi, T., Tanahashi, M., and Naganuma, T. (2007). Phylo-genetic diversity and distribution of dissimila- tory sulfite reductase genes from deep-sea sediment cores. Mar. Biotechnol. 9, 429-436.
31. Knittel, K., Boetius, A., Eilers, H., Lochte, K., Pfannkuche, O., Linke, P., and Amann, R. (2003). Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia margin, Oregon). Geomicrobiol. J. 20, 269-294.
32. Knoblauch, C, Jørgensen, B. B., and Harder, J. (1999). Community size and metabolic rates of psychrophilic sulfate-reducing bacteria in Arctic marine sediments. Appl. Environ. Microbiol. 65, 4230-4233.
33. Kondo, R., Purdy, K. J., Silva, S. Q., and Nedwell, D. B. (2007). Spatial dynamics of sulphate-reducing bacterial compositions in sediment along a salinity gradient in a UK estuary. Microbes Environ. 22, 11-19.
34. Kondo, R., Shigematsu, K., and Butani, J. (2004). Rapid enumeration of sulphate-reducing bacteria from aquatic environments using realtime PCR. Plankton Benthos Res. 3, 180-183.
35. Leloup, J., Fossing, H., Kohls, K., Holmkvist, L., Borowski, C., and Jørgensen, B. B. (2009). Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geo-chemical zonation. Environ. Microbiol. 11,1278-1291.
36. Leloup, J., Loy, A., Knab, N. J., Borowski, C., Wagner, M., and Jorgensen, B. B. (2007). Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ. Microbiol. 9, 131-142.
37. Lindberg, E., Albrechtsen, H. J., and Jacobsen, C. S. (2007). Inhibition of real-time PCR in DNA extracts from aquifer sediment. Geomicrobiol. J. 24, 343-352.
38. Liu, X., Bagwell, C. E., Wu, L., Devol, A. H., and Zhou, J. (2003). Molecular diversity of sulfate-reducing bacteria from two different continental margin habitats. Appl. Environ. Microbiol. 69,6073-6081.
39. Loy, A., Kusel, K., Lehner, A., Drake, H. L., and Wagner, M. (2004). Microar-ray and functional gene analyses of sulfate-reducing prokaryotes in low-sulfate, acidic fens reveal cooccurrence of recognized genera and novel lineages. Appl. Environ. Microbiol. 70,6998-7009.
40. Meyer, B., and Kuever, J. (2007). Phy-logeny of the alpha and beta subunits of the dissimilatory adenosine-5'-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes - origin and evolution of the dissimilatory sulfate-reduction pathway. Microbiology 153, 2026-2044.
41. Mußmann, M., Ishii, K, Rabus, R., and Amann, R. (2005). Diversity and vertical distribution of cultured and uncultured deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ. Microbiol. 7, 405-418.
42. Nadkarni, M. A., Martin, E E., Jacques, N. A., and Hunter, N. (2002). Determination of bacterial load by realtime PCR using a broad-range (universal) probe and primers set. Microbiology 148,257-266.
43. Neretin, L. N., Abed, R. M. M., Schippers, A., Schubert, C. J., Kohls, K., and Kuypers,M.M.M. (2007). Inorganic carbon fixation by sulfate-reducing bacteria in the Black Sea water column. Environ. Microbiol. 9, 3019-3024.
44. Neretin, L. N., Schippers, A., Pernthaler, A., Hamann, K., Amann, R., and Jør-gensen, B. B. (2003). Quantification of dissimilatory (bi)sulphite reductase gene expression in Desulfobac-terium autotrophicum using realtime RT-PCR. Environ. Microbiol. 5, 660-671.
45. Nunoura, T., Soffientino, B., Blazejak, A., Kakuta, J., Oida, H., Schippers, A., and Takai, K. (2009). Subseafloor microbial communities associated with rapid turbidite deposition in the Gulf of Mexico continental slope (IODP Expedition 308). FEMS Microbiol. Ecol. 69, 410-424.
46. Parkes, R. J., Webster, G., Cragg, B. A., Weightman, A. J., Newberry, C. J., Ferdelman, T. G., Kallmeyer, J., Jørgensen, B. B., Aiello, I. W., and Fry, J. C(2005). Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436, 390-394.
47. Ravenschlag, K., Sahm, K., Knoblauch, C, Jørgensen, B. B., and Amann, R. (2000). Community structure, cellular rRNA content and activity of sulfate-reducing bacteria in marine Arctic sediments. Appl. Environ. Microbiol. 66, 3592-3602.
48. Riedinger, N., Brunner, B., Formolo, M. J., Solomon, E., Kasten, S., Strasser, M., and Ferdelman, T. G. (2010). Oxidative sulfur cycling in the deep biosphere of the Nankai trough, Japan. Geology 38, 851-854.
49. Sahm, K., Knoblauch, C., and Amann, R. (1999). Phylogenetic affiliation and quantification of psychrophilic sulfate-reducing isolates in marine Arctic sediments. Appl. Environ. Microbiol. 65,3976-3981.
50. Schen, Y., Buick, R., and Canfield, D. E. (2001). Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature AW, 77-81.
51. Schippers, A., and Jørgensen, B. B. (2001). Oxidation of pyrite and iron sulfide by manganese dioxide in marine sediments. Geochim. Cos-mochim. Acta 65, 915-922.
52. Schippers, A., Köweker, G., Höft, C., and Teichert, B. (2010). Quantification of microbial communities in three forearc sediment basins off Sumatra. Geomicrobiol. J. 27,170-182.
53. Schippers, A., and Neretin, L. N. (2006). Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using realtime PCR. Environ. Microbiol. 8, 1251-1260.
54. Schippers, A., Neretin, L. N., Kallmeyer, J., Ferdelman, T. G., Cragg, B. A., Parkes, R. J., and Jørgensen, B. B. (2005). Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861-864.
55. Sørensen, K. B., and Teske, A. (2006). Stratified communities of active archaea in deep marine subsurface sediments. Appl. Environ. Microbiol. 72,4596-4603.
56. Stahl, D. A., Fishbain, S., Klein, M., Baker, B. J., and Wagner, M. (2002). Origins and diversification of sulfate-respiring microorganisms. Antonie Van Leeuwenhoek 81,189-195.
57. Teske, A. P. (2006). Microbial community composition in deep marine subsurface sediments of ODP Leg 201: sequencing surveys and cultivations. Proc. Ocean Drill. Prog. Sci. Results 201, Available at: http:// www-odp.tamu.edu/publications/201_SR/120/120.htm
58. Teske, A. P., and Sørensen, K. B. (2008). Uncultured archaea in deep marine marine subsurface sediments: have we caught them all? The ISME J. 2, 3-18.
59. Thamdrup, B., Rosselló-Mora, R., and Amann, R. (2000). Microbial manganese and sulfate reduction in Black Sea shelf sediments. Appl. Environ. Microbiol. 66, 2888-2897.
60. Vaerman, J. L., Saussoy, P., and Ingargi-ola, I. (2004). Evaluation of real-time PCR data. J. Biol. Regul. Homeost. Agents 18,212-214.
61. van der Maarel, M. J. E. C., van Bergeijk, S., van Werkhoven, A. E, Laverman, A. M., Meijer, W. G., Stam, W T., and Hansen, T. A. (1996). Cleavage of dimethyl-sulfoniopropionate and reduction of acrylate by Desulfovibrio acryli-cus sp. nov. Arch. Microbiol. 166, 109-115.
62. Vandieken, V., Finke, N., and Jør-gensen, B. B. (2006). Pathways of carbon oxidation in an Arctic fjord sediment (Svalbard) and isolation of psychrophilic and psychrotolerant Fe(III)-reducing bacteria. Mar. Ecol. Prog. Ser. 322, 29-41.
63. Vetriani, C., Tran, H. V., and Kerk-hof, L. J. (2003). Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl. Environ. Microbiol. 69, 6481-6488.
64. Wagner, M., Roger, A. J., Flax, J. L., Brusseau, G. A., and Stahl, D. A. (1998). Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 180,2975-2982.
65. Webster, G., Blazejak, A., Cragg, B. A., Schippers, A., Sass, H., Rinna, J., Tang, X., Mathes, F., Ferdelman, T., Fry, J. C., Weightman, A. J., and Parkes, R. J. (2009). Subsurface microbiology and biogeochem-istry of a deep, cold-water carbonate mound from the Porcupine Seabight (IODP Expedition 307). Environ. Microbiol. 11,239-257.
66. Webster, G., Newberry, C. J., Fry, J. C., and Weightman, A. J. (2003). Assessment of bacterial communitystructure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J. Micro-biol. Methods 55, 155-164.
67. Webster, G., Watt, L. C., Rinna, J., Fry, J. C., Evershed, R. P., Parkes, J., and Weightman, A, J. (2006). A comparison of stable-isotope probing of DNA and phospholipid fatty acids to study prokaryotic functional diversity in sulfate-reducing marine sediment enrichment slurries. Environ. Microbiol. 8,1575-1589.
68. Wilms, R., Sass, H., Köpke, B., Cypionka, H., and Engelen, B. (2007). Methane and sulfate profiles within the subsurface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea. FEMS Microbiol. Ecol. 59, 611-621.