Reverse-transcriptional gene expression of anammox and ammonia-oxidizing archaea and bacteria in soybean and rice paddy soils of Northeast China

Applied Microbiology and Biotechnology

Volumn 98, Issue 6, 2014, Pages 2675-2686

  Wang, Jing ^a,b   Dong, Hailiang ^c,d   Wang, Weidong ^e   Gu, Ji Dong ^b,f  

^a TIANJIN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c China University of Geosciences   (China)

^d MIAMI UNIVERSITY   (United States)

^e HEILONGJIANG BAYI AGRICULTURAL UNIVERSITY   (China)

^f UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Anammox; AOA; AOB; Baijiang soil; Crop rotation; Gene expression; mRNA; Reverse transcription; Rice paddy

Indexed keywords

ANAMMOX; AOA; AOB; CROP ROTATION; MRNA; REVERSE TRANSCRIPTION; RICE PADDY;

AMMONIA; BACTERIA; CULTIVATION; ELECTROPHORESIS; GENE EXPRESSION; GENES; METADATA; NITROGEN; POLYMERASE CHAIN REACTION; SOILS; TRANSCRIPTION; WASTEWATER TREATMENT;

NITROGEN REMOVAL;

AMMONIA; HYDRAZINE; MESSENGER RNA; NITROGEN; OXIDOREDUCTASE; UNSPECIFIC MONOOXYGENASE;

ADAPTATION; AGRICULTURAL SOIL; AMMONIUM; COMMUNITY DYNAMICS; GENE EXPRESSION; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; NITROGEN; OXIDATION; PADDY FIELD; POLYMERASE CHAIN REACTION; SEPARATION; SOYBEAN; TRANSFORMATION;

AGRICULTURE; AMMONIA OXIDIZING ARCHAEON; AMMONIA OXIDIZING BACTERIUM; ANAMMOX BACTERIUM; ARTICLE; BACTERIAL GENE; CHINA; COMMUNITY; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; ENVIRONMENTAL FACTOR; FUNGAL GENE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; RICE PADDY; SOIL; SOYBEAN; TILLAGE;

CHINA; HEILONGJIANG; SANJIANG PLAIN;

AMMONIA; ARCHAEA; BACTERIA; CHINA; DNA, ARCHAEAL; DNA, BACTERIAL; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; OXIDATION-REDUCTION; OXIDOREDUCTASES; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SOYBEANS;

EID: 84896874330     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5242-x     Document Type: Article

References (69)

1. Aakra A, Hesselsoe M, Bakken IR (2000) Surface attachment of ammonia-oxidizing bacteria in soil. Microbiol Ecol 39:222-235 (Pubitemid 30454198)
2. Avrahami S, Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microbiol 69:6152-6164 (Pubitemid 37280341)
3. Aoi Y, Masaki Y, Tsuneda S, Hirata A (2004) Quantitative analysis of amoA mRNA expression as a new biomarker of ammonia oxidation activities in a complex microbial community. Lett Appl Microbiol 39:477-482 (Pubitemid 39577589)
4. Cao H, Li M, Dang H, Gu J-D (2011a) Responses of aerobic and anaerobic ammonia/ammonium-oxidizing microorganisms to anthropogenic pollution in coastal marine environments. Method Enzymol 496:35-62
5. Cao H, Li M, Hong Y, Gu J-D (2011b) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34:513-523
6. Cao H, Hong Y, Li M, Gu J-D (2011c) Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River Estuary to the South China Sea. Anton Leeuw Int J G 100:545-556
7. Cao H, Hong Y, Li M, Gu J-D (2011d) Phylogenetic diversity and ecological pattern of ammonia-oxidizing archaea in the surface sediments of the Western Pacific. Microb Ecol 62:813-823
8. Cao H, Hong Y, Li M, Gu J-D (2012a) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl Microbiol Biotechnol 94:247-259
9. Cao H, Hong Y, Li M, Gu J-D (2012b) Lower abundance of ammonia-oxidizing archaea than ammonia-oxidizing bacteria in the subsurface sediments of the northern South China Sea. Geomicrobiol J 29:1-8
10. Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10:1978-1987
11. Chu HY, Morimoto S, Fujii T, Yagi K, Nishimura S (2009) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Sci Soc Am J 73(6):2026-2031
12. Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11:1194-1207
13. Davis KER, Joseph SJ, Janssen PH (2005) Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Appl Environ Microbiol 71:826-834 (Pubitemid 40223569)
14. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621-629
15. Diab S, Kochba M, Mires D, Avnimelech Y (1992) Combined intensive-extensive (CIE) pond system A: inorganic nitrogen transformations. Aquaculture 101:33-35
16. Egli K, Fanger U, Alvarez PJ, Siegrist H, van der Meer JR, Zehnder AJ (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175:198-207 (Pubitemid 32247230)
17. Francis CA, O'Mullan GD, Ward BB (2003) Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1:129-140
18. 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 (Pubitemid 41457116)
19. Freitag TE, Prosser JI (2003) Community structure of ammonia-oxidizing bacteria within anoxic marine sediments. Appl Environ Microbiol 69:1359-1371 (Pubitemid 36314269)
20. Freitag TE, Prosser JI (2004) Differences between betaproteobacterial ammonia-oxidizing communities in marine sediments and those in overlying water. Appl Environ Microbiol 70:3789-3793 (Pubitemid 38745938)
21. Glasel JA (1995) Validity of nucleic acid purities monitored by 260 nm/280 nm absorbance ratio. Biothech 18:62-63
22. Han P, Gu J-D (2013) More refined diversity of anammox bacteria recovered and distribution in different ecosystems. Appl Microbiol Biotechnol 97:3653-3663
23. Han P, Li M, Gu J-D (2013) Biases in community structures of ammonia/ammonium-oxidizing microorganisms caused by insufficient DNA extractions from Baijiang soil revealed by comparative analysis of coastal wetland sediment and rice paddy soil. Appl Microbiol Biotechnol. doi:10.1007/s00253-013-5169-2
24. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364-2374
25. Herrmann M, Hädrich A, Küsel K (2012) Predominance of thaumarchaeal ammonia oxidizer abundance and transcriptional activity in an acidic fen. Environ Microbiol 14:3013-3025
26. Hooper AT, Vannelli DB, Arciero D (1997) Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Van Leeuwenhoek 71:59-67
27. Hulth S, Aller RC, Gilbert F (1999) Coupled anoxic nitrification/ manganese reduction in marine sediments. Geochim Cosmochim Acta 63:49-66 (Pubitemid 29380951)
28. Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. The ISME J 4:450-454
29. Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658-1671
30. Jiang H, Dong H, Yu B, Lv G, Deng S, Nicole B, Dai M (2009) Diversity and abundance of ammonia-oxidizing archaea and bacteria in Qinghai Lake, Northwestern China. Geomicrobiol J 26:199-211
31. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJM, Harhangi HR, Janssen-Megens EM, Francoijs K-J, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127-130
32. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann Rev Microbiol 55:485-529 (Pubitemid 32978114)
33. Krsek M, Gaze WH, Morris NZ, Wellington EMH (2006) Gene detection, expression and related enzyme activity in soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin, pp 217-255
34. Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299-306 (Pubitemid 351890826)
35. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MMM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci U S A 104:7104-7109 (Pubitemid 47186016)
36. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-809 (Pubitemid 44258909)
37. Li H, Chen S, Mu BZ, Gu J-D (2010a) Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs. Microb Ecol 60:771-783
38. Li H, Mu BZ, Jiang Y, Gu J-D (2011a) Production processes affect prokaryotic amoA gene abundance and distribution in high-temperature petroleum reservoirs. Geomicrobiol J 28:692-704
39. Li M, Cao H, Hong Y, Gu J-D (2011b) Seasonal dynamics of anammox bacteria in estuarial sediments of Mai Po Nature Reserve revealed by 16S rRNA and hzo genes analysis. Microbes Environ 26:15-22
40. Li M, Cao H, Hong Y, Gu J-D (2011c) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243-1254
41. Li M, Hong Y, Klotz MG, Gu J-D (2010b) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86:781-790
42. Lüdemann H, Arth I, Liesack W (2000) Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Appl Environ Microbiol 66:754-762 (Pubitemid 30082770)
43. McTavish H, Fuchs J, Hooper A (1993) Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol 175:2436-2444 (Pubitemid 23123520)
44. Metcalfe AC, Krsek M, Gooday GW, Prosser JI, Wellington EM (2002) Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl Environ Microbiol 68:5042-5050 (Pubitemid 35154816)
45. Milner MG, Curtis TP, Davenport RJ (2008) Presence and activity of ammonia-oxidizing bacteria detected amongst the overall bacterial diversity along a physico-chemical gradient of a nitrifying wastewater treatment plant. Water Res 42:2863-2872
46. Miskin IP, Farrimond P, Head IM (1999) Identification of novel bacterial lineages as active members of the microbial populations in a freshwater sediment using rapid RNA extraction procedure and RT-PCR. Microbiol 145:1977-1987 (Pubitemid 29396928)
47. Mulder A, van de Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177-184
48. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (eds) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 743-770
49. Nicol GW, Glover LA, Prosser JI (2003) Spatial analysis of archaeal community structure in grassland soil. Appl Environ Microbiol 69:7420-7429 (Pubitemid 38585397)
50. Onodera Y, Nnakagawa T, Takahashi R, Tokuyama T (2010) Seasonal change in vertical distribution of ammonia-oxidizing archaea and bacteria and their nitrification in temperate forest soil. Microbes Environ 25:28-35
51. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002-2007
52. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130-3139
53. Roling WF, Milner MG, Jones DM, Fratepietro F, Swannell RPJ, Daniel F, Head IM (2004) Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl Environ Microbiol 70:2603-2613 (Pubitemid 38657769)
54. Rotthauwe J, Witzel K, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704-4712 (Pubitemid 27524201)
55. Saleh-Lakhaa S, Millera M, Campbellb RG, Schneiderc K, Elahimaneshd P, Harta MM, Trevorsa JT (2005) Microbial gene expression in soil: methods, applications and challenges. J Microbiol Methods 63:1-19
56. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM (2008) Pommerening-Roeser A, op den Camp HJM, Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10:3140-3149
57. Schwieger F, Tebbe CC (1998) A new approach to utilize PCR single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870-4876 (Pubitemid 28557853)
58. Stephen JR, Kowalchuk GA, Bruns M-AV, McCaig AE, Phillips CJ, Embley TM, Prosser JI (1998) Analysis of β-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64:2958-2965 (Pubitemid 28363168)
59. Taras MJ (1995) Standard methods for the examination of water and wastewater. American Public Health Association, Washington
60. van de Graaf AA, Mulder A, de Bruijn P, Jetten MS, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61:1246-1251
61. 31P NMR. Appl Microbiol Biotechnol 86:311-317
62. Wang J, Gu J-D (2013a) Dominance of Candidatus Scalindua species in anammox community revealed in soils with different duration of rice paddy cultivation in Northeast China. Appl Microbiol Biotechnol 99:1785-1798
63. Wang Y, Gu J-D (2013b) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97:7015-7033
64. Wagner M, Horn M, Daims H (2003) Fluorescent in situ hybridisation for the identification and characterisation of prokaryotes. Curr Opin Microbiol 6:302-309 (Pubitemid 36841675)
65. Watson SW, Bock E, Harms H, Koops HP, Hooper AA (1989) Nitrifying bacteria. In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey's manual of systematic microbiology, vol 3. Williams and Wilkins, Baltimore, pp 1808-1834
66. Wuchter CB, Abbas MJL, Coolen L, Herfort J, van Bleijswijk P, Timmers M, Strous E, Teira GJ, Herndl JJ, Middelburg S, Schouten JS, Damste S (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103:12317-12322
67. Xing B, Dudas MJ, Zhang Z, Xu Q (1994) Pedogenetic characteristics of albic soils in the three river plain, Heilongjiang Province. Acta Pedologica Sinica 31:95-104
68. Zeng ZS, Xu Q, Gao ZQ (1997) Albic soil in China. Scientific Publishing House, Beijing
69. Zhu G, Wang S, Wang Y, Wang C, Risgaard PN, Jetten MSM, Yin C (2011) Anaerobic ammonia oxidation in a fertilized paddy soil. The ISME J 5:1905-1912