amoA gene abundances and nitrification potential rates suggest that benthic ammonia-oxidizing bacteria and not archaea dominate N cycling in the Colne estuary, United Kingdom

Applied and Environmental Microbiology

Volumn 81, Issue 1, 2015, Pages 159-165

  Li, Jialin ^a,b,c   Nedwell, David B ^a   Beddow, Jessica ^a   Dumbrell, Alex J ^a   McKew, Boyd A ^a   Thorpe, Emma L ^a   Whitby, Corinne ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b OCEAN UNIVERSITY OF CHINA   (China)

^c YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIA; ELECTROPHORESIS; GENES; MICROORGANISMS; NITRIFICATION; OXIC SEDIMENTS;

AMMONIA CONCENTRATIONS; AMMONIA MONOOXYGENASE; AMMONIA OXIDIZERS; AMMONIA OXIDIZING ARCHAEA (AOA); AMMONIA OXIDIZING BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESES (DGGE); ESTUARINE SEDIMENTS; SEQUENCE ANALYSIS;

ESTUARIES;

ABUNDANCE; AMMONIA; BENTHOS; DOMINANCE; ESTUARINE ECOSYSTEM; GENE EXPRESSION; MARINE SEDIMENT; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; NITRIFICATION; NITROGEN CYCLE; OXIC SEDIMENT; SPECIES DIVERSITY;

COLNE ESTUARY; ENGLAND; ESSEX [ENGLAND]; UNITED KINGDOM;

NITROSOMONADALES; NITROSOMONAS;

AMMONIA; AMMONIA MONOOXYGENASE; OXIDOREDUCTASE;

ARCHAEON; BACTERIUM; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; ESTUARY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NITRIFICATION; OXIDATION REDUCTION REACTION; SEASON; SEDIMENT; UNITED KINGDOM;

AMMONIA; ARCHAEA; BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; ESTUARIES; GEOLOGIC SEDIMENTS; GREAT BRITAIN; MOLECULAR SEQUENCE DATA; NITRIFICATION; OXIDATION-REDUCTION; OXIDOREDUCTASES; SEASONS; SEQUENCE ANALYSIS, DNA;

EID: 84917677469     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02654-14     Document Type: Article

References (50)

1. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W. 2004. Environmental shotgun sequencing of the Sargasso Sea. Science 304:66-74. http://dx.doi.org/10.1126/science.1093857.
2. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. 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. http://dx.doi.org/10.1073/pnas.0506625102.
3. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-809. http://dx.doi.org/10.1038/nature04983.
4. Mosier AC, Francis CA. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002-3016. http://dx.doi.org/10.1111/j.1462-2920.2008.01764.x.
5. De Corte D, Yokokawa T, Varela MA, Agogué H, Herndl GJ. 2009. Spatial distribution of Bacteria and Archaea and amoA gene copy numbers throughout the water column of the Eastern Mediterranean Sea. ISME J 3:147-158. http://dx.doi.org/10.1038/ismej.2008.94.
6. Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT. 2007. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660-662. http://dx.doi.org/10.1038/ismej.2007.79.
7. Sahan E, Muyzer G. 2008. Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol Ecol 64:175-186. http://dx.doi.org/10.1111/j.1574-6941.2008.00462.x.
8. Bernhard AE, Landry ZC, Blevins A, de la Torre JR, Giblin AE, Stahl DA. 2010. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76:1285-1289. http://dx.doi.org/10.1128/AEM.02018-09.
9. Bernhard AE, Tucker J, Giblin AE, Stahl DA. 2007. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ Microbiol 9:1439-1447. http://dx.doi.org/10.1111/j.1462-2920.2007.01260.x.
10. Ogilvie B, Nedwell DB, Harrison RM, Robinson A, Sage A. 1997. High nitrate, muddy estuaries as nitrogen sinks: the nitrogen budget of the River Colne estuary (United Kingdom). Mar Ecol Progr Ser 150:217-228. http://dx.doi.org/10.3354/meps150217.
11. Papaspyrou S, Smith CJ, Dong LF, Whitby C, Dumbrell AJ, Nedwell DB. 2014. Nitrate reduction functional genes and nitrate reduction potentials persist in deeper estuarine sediments. Why? PLoS One 9:e94111. http://dx.doi.org/10.1371/journal.pone.0094111.
12. Dong LF, Thornton DCO, Nedwell DB, Underwood GJC. 2000. Denitrification in sediments of the River Colne estuary, England. Mar Ecol Progr Ser 203:109-122. http://dx.doi.org/10.3354/meps203109.
13. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976-979. http://dx.doi.org/10.1038/nature08465.
14. Di HJ, Cameron KC, Shen J-P, Winefield CS, O'Callaghan M, Bowatte S, He J-Z. 2010. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386-394. http://dx.doi.org/10.1111/j.1574-6941.2010.00861.x.
15. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific subtropical gyre. Environ Microbiol 9:1162-1175. http://dx.doi.org/10.1111/j.1462-2920.2007.01239.x.
16. Bernhard AE, Donn T, Giblin AE, Stahl DA. 2005. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ Microbiol 7:1289-1297. http://dx.doi.org/10.1111/j.1462-2920.2005.00808.x.
17. Strickland JDH, Parsons TR. 1972. A practical handbook of seawater analysis, 2nd ed. Fisheries Research Board of Canada, Ottawa, Ontario, Canada.
18. Berges JA, Franklin DJ, Harrison PJ. 2004. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades (Corrigendum). J Phycol 40:619-619. http://dx.doi.org/10.1111/j.1529-8817.2004.40301.x.
19. Dollhopf SL, Hyun JH, Smith AC, Adams HJ, O'Brien S, Kostka JE. 2005. Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Appl Environ Microbiol 71: 240-246. http://dx.doi.org/10.1128/AEM.71.1.240-246.2005.
20. Pai SC, Tsau YJ, Yang TI. 2001. pH and buffering capacity problems involved in the determination of ammonia in saline water using the indophenol blue spectrophotometric method. Anal Chim Acta 434:209-216. http://dx.doi.org/10.1016/S0003-2670(01)00851-0.
21. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ. 2000. Rapid method for co-extraction of DNA and RNA from natural environments for analysis of ribosomal DNA-and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488-5491. http://dx.doi.org/10.1128/AEM.66.12.5488-5491.2000.
22. Nicol GW, Tscherko D, Embley TM, Prosser JI. 2005. Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7:337-347. http://dx.doi.org/10.1111/j.1462-2920.2005.00698.x.
23. Rotthauwe JH, Witzel KP, Liesack W. 1997. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of national ammonia-oxidizing population. Appl Environ Microbiol 63:4704-4712.
24. Tourna M, Freitag TE, Nicol GW, Prosser JI. 2008. Growth, activity and temperature responses of ammonia-oxidising archaea and bacteria in soil microcosms. Environ Microbiol 10:1357-1364. http://dx.doi.org/10.1111/j.1462-2920.2007.01563.x.
25. Kowalchuk GA, Stephen JR, Deboer W, Prosser JI, Embley TM, Woldendorp JW. 1997. Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Appl Environ Microbiol 63:1489-1497.
26. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ. 2007. Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165-176. http://dx.doi.org/10.1111/j.1462-2920.2006.01125.x.
27. Muyzer G, De Wall EC, Uitterlinden AG. 1993. Profiling of complex microbial population by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700.
28. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genome Sciences, University of Washington, Seattle, WA.
29. Jukes TH, Cantor CR. 1969. Mammalian protein metabolism. Academic Press, New York, NY.
30. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
31. Page R. 1996. Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357-358.
32. Ishak HD. 2011. Bacterial diversity in Solenopis invicta and Solenopsis geminate ant colonies characterized by 16S amplicon 454 pyrosequencing. Microb Ecol 61:821-831. http://dx.doi.org/10.1007/s00248-010-9793-4.
33. Takai K, Horikoshi K. 2000. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066-5072. http://dx.doi.org/10.1128/AEM.66.11.5066-5072.2000.
34. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pentilde AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
35. Edgar R. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
36. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261-5267. http://dx.doi.org/10.1128/AEM.00062-07.
37. Dickie IA. 2010. Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol 188:916-918. http://dx.doi.org/10.1111/j.1469-8137.2010.03473.x.
38. Development Core Team R. 2007. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
39. Norusis MJ. 2010. PASW statistics 18 guide to data analysis. Prentice-Hall, New York, NY.
40. Kuenen JG, Robertson LA. 1987. Ecology of nitrification and denitrification, p 162-218. In Cole JA, Ferguson SJ (ed), The nitrogen and sulphur cycles. Cambridge University Press, Cambridge, United Kingdom.
41. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeota from a hot spring. Proc Natl Acad Sci USA 105:2134-2139. http://dx.doi.org/10.1073/pnas.0708857105.
42. Shen T, Stieglmeier M, Dai J, Urich T, Schleper C. 2013. Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol Lett 344:121-129. http://dx.doi.org/10.1111/1574-6968.12164.
43. de Bie MJM, Speksnijder AGCL, Kowalchuk GA, Schuurman T, Zwart G, Stephen JR, Diekmann OE, Laanbroek HJ. 2001. Shifts in the dominant populations of ammonia-oxidizing β-subclass Proteobacteria along the eutrophic Schelde estuary. Aquat Microb Ecol 23:225-236. http://dx.doi.org/10.3354/ame023225.
44. Verhamme DT, Prosser JI, Nicol GW. 2011. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067-1071. http://dx.doi.org/10.1038/ismej.2010.191.
45. Thornton DCO, Dong LF, Underwood GCU, Nedwell DB. 2002. Factors affecting microphytobenthos biomass, species composition and production in the Colne Estuary (UK). Aquat Microb Ecol 27:285-300. http://dx.doi.org/10.3354/ame027285.
46. Cébron A, Berthe T, Garnier J. 2003. Nitrification and nitrifying bacteria in the lower Seine River and estuary (France). Appl Environ Microbiol 69:7091-7100. http://dx.doi.org/10.1128/AEM.69.12.7091-7100.2003.
47. + adsorption capacity, nitrification, and denitrification in Danish estuarine sediments. Estuaries 22:21-30. http://dx.doi.org/10.2307/1352923.
48. Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA. 2004. Competition between ammonia-oxidizing bacteria and benthic microalgae. Appl Environ Microbiol 70:5528-5537. http://dx.doi.org/10.1128/AEM.70.9.5528-5537.2004.
49. Seitzinger SP, Gardner WS, Spratt AK. 1991. The effect of salinity on ammonium sorption in aquatic sediments-implications for benthic nutrient recycling. Estuaries 14:167-174. http://dx.doi.org/10.2307/1351690.
50. Smith CJ, Nedwell DB, Dong LF, Osborn AM. 2007. Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612-3622. http://dx.doi.org/10.1128/AEM.02894-06.