Abundance and diversity based on amoA genes of ammonia-oxidizing archaea and bacteria in ten wastewater treatment systems

Applied Microbiology and Biotechnology

Volumn 98, Issue 7, 2014, Pages 3339-3354

  Gao, Jingfeng ^a   Luo, Xin ^a   Wu, Guixia ^a   Li, Ting ^a   Peng, Yongzhen ^a  

^a BEIJING UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Ammonia oxidizing archaea (AOA); Ammonia oxidizing bacteria (AOB); amoA gene; Wastewater treatment systems (WTSs)

Indexed keywords

AMMONIA; EFFLUENTS; GENES; NITROGEN REMOVAL; POLYMERASE CHAIN REACTION; RECLAMATION; WASTEWATER TREATMENT;

AMMONIA OXIDATION; AMMONIA OXIDIZING BACTERIA; AMMONIA-OXIDIZING ARCHAEA; DOMINANT SPECIES; NITROSOMONAS EUROPAEA; PHYLOGENETIC ANALYSIS; QUANTITATIVE REAL TIME PCR; WASTEWATER TREATMENT SYSTEM;

BACTERIA;

AMMONIA;

ABUNDANCE; AMMONIA; COEXISTENCE; DOMINANCE; GENETIC ANALYSIS; MICROBIAL ECOLOGY; OXIDATION; PHYLOGENETICS; PROKARYOTE; SEWAGE TREATMENT; SPECIES DIVERSITY;

AMMONIA OXIDIZER; AMMONIA OXIDIZING ARCHAEON; AMMONIA OXIDIZING BACTERIUM; AMOA GENE; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; COMMUNITY STRUCTURE; CONTROLLED STUDY; GENE DOSAGE; GENE SEQUENCE; LIMIT OF DETECTION; MICROBIAL DIVERSITY; MOLECULAR CLONING; NITROSOCALDUS; NITROSOMONAS; NITROSOMONAS EUROPAEA; NITROSOMONAS OLIGOTROPHA; NITROSOPUMILUS; NITROSOSPHAERA; NITROSOSPHAERA SISTER; NITROSOTALEA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; WASTE WATER MANAGEMENT;

CANDIDATUS NITROSOPUMILUS; NITROSOMONADALES; NITROSOMONAS; NITROSOMONAS EUROPAEA; NITROSOMONAS OLIGOTROPHA;

AMMONIA; ARCHAEA; BACTERIA; BIOTA; DNA, ARCHAEAL; DNA, BACTERIAL; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; WASTE WATER;

EID: 84898925145     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5428-2     Document Type: Article

References (64)

1. Abeliovich A, Vonshak A (1992) Anaerobic metabolism of Nitrosomonas-europaea. Arch Microbiol 158:267-270
2. Arp D, Sayavedra-Soto L, Hommes N (2002) Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch Microbiol 178:250-255
3. Bae H, Chung YC, Jung JY (2010) Microbial community structure and occurrence of diverse autotrophic ammonium oxidizing microorganisms in the anammox process. Water Sci Technol 61:2723-2732
4. Bai Y, Sun Q, Wen D, Tang X (2012) Abundance of ammonia-oxidizing bacteria and archaea in industrial and domestic wastewater treatment systems. FEMS Microbiol Ecol 80:323-330
5. Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico. Appl Environ Microbiol 72:7767-7777
6. Coolen MJL, Abbas B, Van Bleijswijk J, Hopmans EC, Kuypers MMM, Wakeham SG, Sinninghe Damsté JS (2007) Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ Microbiol 9:1001-1016
7. Coskuner G, Curtis TP (2002) In situ characterization of nitrifiers in an activated sludge plant: detection of Nitrobacter spp. J Appl Microbiol 93:431-437
8. de Vet WWJM, Dinkla IJT, Muyzer G, Rietveld LC, van Loosdrecht MCM (2009) Molecular characterization of microbial populations in groundwater sources and sand filters for drinking water production. Water Res 43:182-194
9. Ducey TF, Vanotti MB, Shriner AD, Szogi AA, Ellison AQ (2010) Characterization of a microbial community capable of nitrification at cold temperature. Bioresour Technol 101:491-500
10. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855-869
11. 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
12. Fukushima T, Wu YJ, Whang LM (2012) The influence of salinity and ammonium levels on amoA mRNA expression of ammonia-oxidizing prokaryotes. Water Sci Technol 65:2228-2235
13. Gao JF, Luo X, Wu GX, Li T, Peng YZ (2013) Quantitative analyses of the composition and abundance of ammonia-oxidizing archaea and ammonia-oxidizing bacteria in eight full-scale biological wastewater treatment plants. Bioresour Technol 138:285-296
14. Gieseke A, Purkhold U, Wagner M, Amann R, Schramm A (2001) Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl Environ Microbiol 67:1351-1362
15. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (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
16. Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen U, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG (1998) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421-437
17. Jin T, Zhang T, Yan Q (2010) Characterization and quantification of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in a nitrogen-removing reactor using T-RFLP and qPCR. Appl Microbiol Biotechnol 87:1167-1176
18. Kayee P, Sonthiphand P, Rongsayamanont C, Limpiyakorn T (2011) Archaeal amoA genes outnumber bacterial amoA genes in municipal wastewater treatment plants in Bangkok. Microb Ecol 62:776-788
19. Kindaichi T, Tsushima I, Ogasawara Y, Shimokawa M, Ozaki N, Satoh H, Okabe S (2007) In situ activity and spatial organization of anaerobic ammonium-oxidizing (Anammox) bacteria in biofilms. Appl Environ Microbiol 73:4931-4939
20. Könneke M, Bernhard AE, De La Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-546
21. Koops HP, Pommerening-Röser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37:1-9
22. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299-306
23. Laanbroek H, Bodelier PE, Gerards S (1994) Oxygen consumption kinetics of Nitrosomonas europaea and Nitrobacter hamburgensis grown in mixed continuous cultures at different oxygen concentrations. Arch Microbiol 161:156-162
24. Lam P, Jensen MM, Lavik G, McGinnis DF, Müller 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
25. Limpiyakorn T, Shinohara Y, Kurisu F, Yagi O (2005) Communities of ammonia-oxidizing bacteria in activated sludge of various sewage treatment plants in Tokyo. FEMS Microbiol Ecol 54:205-217
26. Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polprasert C (2011) Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresour Technol 102:3694-3701
27. Limpiyakorn T, Fürhacker M, Haberl R, Chodanon T, Srithep P, Sonthiphand P (2013) amoA-encoding archaea in wastewater treatment plants: a review. Appl Microbiol Biotechnol 97:1425-1439
28. Lydmark P, Almstrand R, Samuelsson K, Mattsson A, Sörensson F, Lindgren P-E, Hermansson M (2007) Effects of environmental conditions on the nitrifying population dynamics in a pilot wastewater treatment plant. Environ Microbiol 9:2220-2233
29. Ma B, Peng Y, Zhang S, Wang J, Gan Y, Chang J, Wang S, Wang S, Zhu G (2013) Performance of anammox UASB reactor treating low strength wastewater under moderate and low temperatures. Bioresour Technol 129:606-611
30. 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
31. Mobarry BK, Wagner M, Urbain V, Rittmann BE, Stahl DA (1996) Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl Environ Microbiol 62:2156-2162
32. Mußmann M, Brito I, Pitcher A, Sinninghe Damsté JS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Müller A, Daims H, Wagner M, Head IM (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U S A 108:16771-16776
33. Park HD, Noguera DR (2004) Evaluating the effect of dissolved oxygen on ammonia-oxidizing bacterial communities in activated sludge. Water Res 38:3275-3286
34. Park HD, Wells GF, Bae H, Griddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643-5647
35. Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damsté JS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76:7575-7587
36. Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) AmoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525-539
37. Poth M (1986) Dinitrogen production from nitrite by a nitrosomonas isolate. Appl Environ Microbiol 52:957-959
38. Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66(12):5368-5382
39. Ritchie GA, Nicholas DJ (1972) Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochem J 126:1181-1191
40. Rodriguez-Caballero A, Hallin S, Pahlson C, Odlare M, Dahlquist E (2012) Ammonia oxidizing bacterial community composition and process performance in wastewater treatment plants under low temperature conditions. Water Sci Technol 65(2):197-204
41. Rotthauwe JH, Witzel KP, 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
42. Rowan AK, Snape JR, Fearnside D, Barer MR, Curtis TP, Head IM (2003) Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. FEMS Microbiol Ecol 43:195-206
43. 2O produced by marine ammonia-oxidizing archaea. Science 333:1282-1285
44. Sauder LA, Peterse F, Schouten S, Neufeld JD (2012) Low-ammonia niche of ammonia-oxidizing archaea in rotating biological contactors of a municipal wastewater treatment plant. Environ Microbiol 14:2589-2600
45. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541
46. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93-106
47. Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214-222
48. Siripong S, Rittmann BE (2007) Diversity study of nitrifying bacteria in full-scale municipal wastewater treatment plants. Water Res 41:1110-1120
49. Sofia A, Liu WT, Ong SL, Ng WJ (2004) In-situ characterization of microbial community in an A/O submerged membrane bioreactor with nitrogen removal. Water Sci Technol 50:41-48
50. Sonthiphand P, Limpiyakorn T (2011) Change in ammonia-oxidizing microorganisms in enriched nitrifying activated sludge. Appl Microbiol Biotechnol 89:843-853
51. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, Schleper C (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331-340
52. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420-8425
53. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985-1995
54. van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142:2187-2196
55. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74
56. Wang S, Zhu G, Peng Y, Jetten MSM, Yin C (2012) Anammox bacterial abundance, activity, and contribution in riparian sediments of the Pearl River estuary. Environ Sci Technol 46:8834-8842
57. Wells GF, Park HD, Yeung CH, Eggleston B, Francis CA, Criddle CS (2009) Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ Microbiol 11:2310-2328
58. Woebken D, Fuchs BM, Kuypers MMM, Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73:4648-4657
59. Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723-1732
60. Wu YJ, Whang LM, Fukushima T, Chang SH (2013) Responses of ammonia-oxidizing archaeal and betaproteobacterial populations to wastewater salinity in a full-scale municipal wastewater treatment plant. J Biosci Bioeng 115:424-432
61. Ye L, Zhang T (2011) Ammonia-oxidizing bacteria dominates over ammonia-oxidizing archaea in a saline nitrification reactor under low DO and high nitrogen loading. Biotechnol Bioeng 108:2544-2552
62. Zhang T, Jin T, Yan Q, Shao M, Wells G, Criddle C, Fang HHP (2009) Occurrence of ammonia-oxidizing Archaea in activated sludges of a laboratory scale reactor and two wastewater treatment plants. J Appl Microbiol 107:970-977
63. Zhang T, Ye L, Tong A, Shao M-F, Lok S (2011) Ammonia-oxidizing archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors. Appl Microbiol Biotechnol 91:1215-1225
64. Zhu G, Wang S, Feng X, Fan G, Jetten MSM, Yin C (2011) Anammox bacterial abundance, biodiversity and activity in a constructed wetland. Environ Sci Technol 45:9951-9958