Seasonal variation in denitrification and dissimilatory nitrate reduction to ammonia process rates and corresponding key functional genes along an estuarine nitrate gradient

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Smith, Cindy J ^a,b,d   Dong, Liang F ^a   Wilson, John ^b   Stott, Andrew ^c   Osborn, A Mark ^b,e   Nedwell, David B ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^e RMIT UNIVERSITY   (Australia)

Author keywords

(RT) Q PCR; Denitrification DNRA; napA; narG; nirS; nrfA

Indexed keywords

NITRATE REDUCTASE; OXIDOREDUCTASE; RNA 16S;

AMMONIA FORMATION; ARTICLE; COMMUNITY STRUCTURE; DENITRIFICATION; ENZYME ACTIVITY; ESTUARINE SPECIES; GENETIC TRANSCRIPTION; MULTIDIMENSIONAL SCALING; NONHUMAN; NUCLEIC ACID ANALYSIS; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEASONAL VARIATION; SPECIES DIVERSITY; WATER TEMPERATURE;

BACTERIA (MICROORGANISMS);

EID: 84936991954     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00542     Document Type: Article

References (52)

1. Abell, G. C. J., Revill, A. T., Smith, C., Bissett, A. P., Volkman, J. K., and Robert, S. S. (2010). Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J. 4, 286-300. doi: 10.1038/ismej.2009.105
2. Brin, L. D., Giblin, A. E., and Rich, J. J. (2014). Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnol. Oceangr. 59, 851-860. doi: 10.4319/lo.2014.59.3.0851
3. Burgin, A. J., and Hamilton, S. K. (2007). Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front. Ecol. Environ. 5:89-96. doi: 10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2
4. Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117-143. doi: 10.1111/j.1442-9993.1993.tb00438.x
5. Clarke, K. R., and Ainsworth, M. (1993). A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 92, 205-219. doi: 10.3354/meps092205
6. Clarke, K. R., Somerfield, P. J., and Chapman, M. G. (2006). On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330, 55-80. doi: 10.1016/j.jembe.2005.12.017
7. Cornwell, J. C., Kemp, W. M., and Kana, T. M. (1999). Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquat. Ecol. 33, 41-54. doi: 10.1023/A:1009921414151
8. Dong, L. F., Nedwell, D. B., Underwood, G. J. C., Thornton, D. C. O., and Rusmana, I. (2002). Nitrous oxide formation in the Colne estuary, England: the central role of nitrite. Appl. Environ. Microbiol. 68, 1240-1249. doi: 10.1128/AEM.68.3.1240-1249.2002
9. Dong, L. F., Nedwell, D. B., and Stott, A. (2006). Sources of nitrogen used for denitrification and nitrous oxide formation in sediments of the hypernutrified Colne, the nutrified Humber, and the oligotrophic Conwy estuaries, United Kingdom. Limnol. Oceangr. 51, 545-557. doi: 10.4319/lo.2006.51.1_part_2.0545
10. Dong, L. F., Smith, C. J., Papaspyrou, S., Stott, A., Osborn, A. M., and Nedwell, D. B. (2009). Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne estuary, United Kingdom). Appl. Environ. Microbiol. 75, 3171-3179. doi: 10.1128/AEM.02511-08
11. Dong, L. F., Sobey, M. N., Smith, C. J., Rusmana, I., Phillips, W., Stott, A., et al. (2011). Dissimilatory reduction of nitrate to ammonium, not denitrification or anammox, dominates benthic nitrate reduction in tropical estuaries. Limnol. Oceanogr. 56, 279-291. doi: 10.4319/lo.2011.56.1.0279
12. Dong, L. F., Thornton, D., and Nedwell, D. B. (2000). Denitrification in sediments of the River Colne estuary, England. Mar. Ecol. Prog. Ser. 203, 109-122. doi: 10.3354/meps203109
13. Earl, T. J., Upton, G. J. G., and Nedwell, D. B. (2014). UK catchments nutrient loads 1993-2003, a new approach using harmonised monitoring scheme data: temporal changes, geographical distribution, limiting nutrients and loads to coastal waters. Environ. Sci. Process. Impact. 16, 1646-1658. doi: 10.1039/c4em00021h
14. Fulweiler, R., and Heiss, E. (2014). (Nearly) A decade of directly measured sediment N2 fluxes: what can narragansett bay tell us about the global ocean nitrogen budget? Oceanography 27, 184-195. doi: 10.5670/oceanog.2014.22
15. Giblin, A. E., Tobias, C. R., Song, B., Weston, N., and Banta, G. T. (2013). The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26, 124-131. doi: 10.5670/oceanog.2013.54
16. Giblin, A. E., Weston, N. B., Banta, G. T., Tucker, J., and Hopkinson, C. S. (2010). The effects of salinity on nitrogen losses from an oligohaline estuarine sediment. Estuaries Coasts 33, 1054-1068. doi: 10.1007/s12237-010-9280-7
17. Ikeda, E., Andou, S., Iwama, U., Kato, C., Horikoshi, K., and Tamegai, H. (2009). Physiological roles of two dissimilatory nitrate reductases in the deep-sea denitrifier Pseudomonas sp. strain MT-1. Biosci. Biotechnol. Biochem. 73, 896-900. doi: 10.1271/bbb.80833
18. Jørgensen, K. S. (1989). Annual pattern of denitrification and nitrate ammonification in estuarine sediment. Appl. Environ. Microbiol. 55, 1841-1847.
19. Kelly-Gerreyn, B. A., Trimmer, M., and Hydes, D. J. (2001). A diagenetic model discriminating denitrification and dissimilatory nitrate reduction to ammonium in a temperate estuarine sediment. Mar. Ecol. Prog. Ser. 220, 33-46. doi: 10.3354/meps220033
20. King, D., and Nedwell, D. B. (1985). The influence of nitrate concentration upon the end-products of nitrate dissimilation by bacteria in anaerobic salt marsh sediment. FEMS Microbiol. Ecol. 1, 23-28. doi: 10.1111/j.1574-6968.1985.tb01127.x
21. Kraft, B., Tegetmeyer, H. E., Sharma, R., Klotz, M. G., Ferdelman, T. G., Hettich, R. L., et al. (2014). The environmental controls that govern the end product of bacterial nitrate respiration. Science 345, 676-679. doi: 10.1126/science.1254070
22. Kuenen, J. G. (2008). Anammox bacteria: from discovery to application. Nat. Rev. Micro. 6, 320-326. doi: 10.1038/nrmicro1857
23. Lane, D. J. (1991). "16S/23S rRNA sequencing," in Nucleic Acid Techniques in Bacterial Systematics, eds E. Stackebrandt, and M. Goodfellow (Chichester: John Wiley & Sons), 115-175.
24. Lisa, J. A., Song, B., Tobias, C. R., and Duernberger, K. A. (2014). Impacts of freshwater flushing on anammox community structure and activities in the New River Estuary, USA. Aquat. Microb. Ecol. 72, 17-31. doi: 10.3354/ame01682
25. Liu, B., Mørkved, P. T., Frostegård, Å., and Bakken, L. R. (2010). Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol. Ecol. 72, 407-417. doi: 10.1111/j.1574-6941.2010.00856.x
26. Lozupone, C. A., and Knight, R. (2007). Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. U.S.A. 104, 11436-11440. doi: 10.1073/pnas.0611525104
27. Marchesi, J. R., Sato, T., and Weightman, A. J. (1998). Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64, 795-799.
28. Nedwell, D. B., Jickells, T. D., Trimmer, M., and Sanders, R. (1999). "Nutrients in estuaries," in Estuaries Advances in Ecological Research, eds D. B. Nedwell, D. G. Raffaelli, and A. H. Fitter (San Diego: Academic Press), 43-92. doi: 10.1016/S0065-2504(08)60191-9
29. Nedwell, D. B., Dong, L. F., Sage, A., and Underwood, G. J. C. (2002). Variations of the nutrients loads to the mainland U.K. estuaries: correlation with catchment areas, urbanization and coastal eutrophication. Estuar. Coast. Mar. Sci. 54, 951-970. doi: 10.1006/ecss.2001.0867
30. Nicholls, J. C., and Trimmer, M. (2009). Widespread occurrence of the anammox reaction in estuarine sediments. Aquat. Microb. Ecol. 55, 105-113. doi: 10.3354/ame01285
31. Nogales, B., Timmis, K. N., Nedwell, D. B., and Osborn, A. M. (2002). Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl. Environ. Microbiol. 68, 5017-5025. doi: 10.1128/AEM.68.10.5017-5025.2002
32. Ogilvie, B., Nedwell, D. B., Harrison, R. M., Robinson, A., and Sage, A. (1997). High nitrate, muddy estuaries as nitrogen sinks: the nitrogen budget of the River Colne estuary (United Kingdom). Mar. Ecol. Prog. Ser. 150, 217-228. doi: 10.3354/meps150217
33. Papaspyrou, S., Smith, C. J., Dong, L. F., Whitby, C., Dumbrell, A. J., and Nedwell, D. B. (2014). Nitrate Reduction Functional Genes and Nitrate Reduction Potentials Persist in Deeper Estuarine Sediments. Why? PLoS ONE 9:e94111. doi: 10.1371/journal.pone.0094111
34. Philippot, L., and Hallin, S. (2005). Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr. Opin. Microbiol. 8, 234-239. doi: 10.1016/j.mib.2005.04.003
35. Richardson, D. J., Berks, B. C., Russell, D. A., Spiro, S., and Taylor, C. J. (2001). Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell. Mol. Life Sci. 58, 165-178. doi: 10.1007/PL00000845
36. Robinson, A. D., Nedwell, D. B., Harrison, R. M., and Ogilvie, B. G. (1998). Hypernutrified estuaries as sources of N2O emission to the atmosphere: the estuary of the River Colne, Essex, UK. Mar. Ecol. Prog. Ser. 164, 59-71. doi: 10.3354/meps164059
37. Seitzinger, S. P. (1988). Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceangr. 33, 702-724. doi: 10.4319/lo.1988.33.4_part_2.0702
38. Simon, J. (2002). Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol. Rev. 26, 285-309. doi: 10.1111/j.1574-6976.2002.tb00616.x
39. Smith, C. J., Danilowicz, B. S., Clear, A. K., Costello, F. J., Wilson, B., and Meijer, W. G. (2005). T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol. Ecol. 54, 375-380. doi: 10.1016/j.femsec.2005.05.002
40. Smith, C. J., Nedwell, D. B., Dong, L. F., and Osborn, A. M. (2006). Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ. Microbiol. 8, 804-815. doi: 10.1111/j.1462-2920.2005.00963.x
41. Smith, C. J., Nedwell, D. B., Dong, L. F., and Osborn, A. M. (2007). Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl. Environl. Microbiol. 73, 3612-3622. doi: 10.1128/AEM.02894-06
42. Song, B., Lisa, J. A., and Tobias, C. R. (2014). Linking DNRA community structure and activity in a shallow lagoonal estuarine system. Front. Microbiol. 5:460. doi: 10.3389/fmicb.2014.00460
43. Strickland, J. D. H., and Parsons, T. R. (1972). A Practical Handbook of Seawater Analysis, 2nd Edn. Ottawa: Fisheries Research Board of Canada, 310.
44. Strous, M., Fuerst, J. A., Kramer, E. H., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T., et al. (1999). Missing lithotroph identified as new planctomycete. Nature 400, 446-449. doi: 10.1038/22749
45. Suzuki, M. T., Taylor, L. T., and Delong, E. F. (2000). Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl. Environ. Microbiol. 66, 4605-4614. doi: 10.1128/AEM.66.11.4605-4614.2000
46. Thornton, D., Dong, L. F., and Underwood, G. (2007). Sediment-water inorganic nutrient exchange and nitrogen budgets in the Colne Estuary, UK. Mar. Ecol. Prog. Ser. 337, 63-77. doi: 10.3354/meps337063
47. Tiedje, J. M. (1988). "Ecology of denitrification and dissimilatory nitrate reduction to ammonium," in Environmental Microbiology of Anaerobes, ed. A. J. B. Zehnder (New York: Biology of anaerobic microorganisms), 179-244.
48. Trimmer, M., Nedwell, D. B., Sivyer, D. B., and Malcolm, S. J. (1998). Nitrogen fluxes through the lower estuary of the river Great Ouse, England: the role of the bottom sediments. Mar. Ecol. Prog. Ser. 163, 109-124. doi: 10.3354/meps163109
49. Trimmer, M., Nedwell, D. B., Sivyer, D. B., and Malcolm, S. J. (2000). Seasonal benthic organic matter mineralisation measured by oxygen uptake and denitrification along a transect of the inner and outer River Thames estuary, UK. Mar. Ecol. Prog. Ser. 197, 103-119. doi: 10.3354/meps197103
50. Tukey, J. W. (1953). The collected works of John W. Tukey: Multiple Comparisons, 1948-1983, ed. H. Braun (New York: Taylor & Francis).
51. Wuchter, C., Abbas, B., Coolen, M. J. L., Herfort, L., van Bleijswijk, J., Timmers, P., et al. (2006). Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U.S.A. 103, 12317-12322. doi: 10.1073/pnas.0600756103
52. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616.