|Table of Contents|

Progress on ammonia-oxidizing archaea and their response to environmental factors(PDF)

Chinese Journal of Applied & Environmental Biology[ISSN:1006-687X/CN:51-1482/Q]

Issue:
2014 06
Page:
1117-1123
Research Field:
Reviews
Publishing date:

Info

Title:
Progress on ammonia-oxidizing archaea and their response to environmental factors
Author(s):
CHEN Yangwu HU Shuang FANG Lu JIANG Dengmei TAN Zhouliang LI Xudong
1Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China 2Chongqing Banan Environmental Monitoring Station, Chongqing 401320, China
Keywords:
AOA AOB environmental factors ammonia community structure abundance
CLC:
X172
PACS:
DOI:
10.3724/SP.J.1145.2014.003024
DocumentCode:

Abstract:
Ammonia oxidation, the rate-limiting step of nitrification, is widely studied because of its importance to global nitrogen biogeochemical circulation. For more than 100 years ammonia oxidizing bacteria (AOB) has been considered the dominant microbial community for ammonia oxidation. Only recently the enrichment culture technology and molecular biology techniques found that ammonia-oxidizing archaea (AOA) also widely exist in different environments. The discovery of AOA not only perfects the nitrogen cycle, but also provides new directions for the research of ammonia oxidation for its response to different environmental factors. This review summarizes the discovery of archaea ammonia oxidation, focusing on the activity of AOA and its occurrence in salty water environment, fresh water environment, soil environment, sewage systems and extreme environments. It mainly discusses the impacts of AOA community structure and abundance under different environmental factors including ammonia concentration, temperature, salinity, dissolved oxygen and pH. Because of its high affinity to ammonia and oxygen, AOA plays a more important role on poor nutrition, low dissolved oxygen and low pH conditions. Also, AOA could survive a more wider temperature range than AOB. The article also briefly introduces the application of AOA into composting process and the perspective for future research in this field.

References

1 Junier P, Molina V, Dorador C, Hadas O, Kim OS, Junier T, Witzel KP, Imhoff JF. Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment [J]. Appl Microbiol Biotechnol, 2010, 85 (3): 425-440
2 Kowalchuk GA, Stephen JR. Ammonia-oxidizing bacteria: A model for molecular microbial ecology [J]. Annu Rev Microbiol, 2001, 55: 485-529
3 Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: Implications for molecular diversity surveys [J]. Appl Environ Microbiol, 2000, 66 (12): 5368-5382
4 Schleper C, Nicol GW. Ammonia-oxidising archaea—physiology, ecology and evolution [J]. Adv Microb Physiol, 2010, 57: 1-41
5 Brian PH, Jessica KC, Amanda JW, Weiguo H, Enmin Z, Li WJ, Dong H. A review of the microbiology of the Rehai geothermal [J]. Geoscience Front, 2012, 3 (3): 273-288
6 胡安谊, 焦念志. 氨氧化古菌——环境微生物生态学研究的一个前沿热点[J]. 自然科学进展, 2009, 19 (4): 370-379
7 Simon HM, Jahn CE, Bergerud LT, Sliwinski MK, Weimer PJ, Willis DK, Goodman RM. Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots [J]. Appl Environ Microbiol, 2005, 71 (8): 4751-4760
8 Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR [J]. Environ Microbiol, 2003, 5 (9): 787-797
9 Karner MB, DeLong EF, Karl DM. Archaeal dominance in the mesopelagic zone of the Pacific Ocean [J]. Nature, 2001, 409 (6819): 507-510
10 Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, 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. Environmental genome shotgun sequencing of the Sargasso Sea [J]. Science, 2004, 304 (5667): 66-74
11 Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C.Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling [J]. Environ Microbiol, 2005, 7 (12): 1985-1995
12 Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon [J]. Nature , 2005, 437 (7058): 543-546
13 Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, Schleper C. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota [J]. Trends Microbiol, 2010, 18 (8): 331-340
14 Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota [J]. Nat Rev Microbiol, 2008, 6 (3): 245-252
15 Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota [J]. Plos Biol, 2006, 4 (4):e95
16 Hayatsu M, Tago K, Saito M. Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification [J]. Soil Sci Plant Nutr, 2008, 54 (1): 33-45
17 Zhang CL, Ye Q, Huang ZL, Chen JW, Song Z, Zhao W, Bagwell C, Inskeep WP, Ross C, Gao L, Wiegel J, Romanek CS, Shock EL, Hedlund BP. Global occurrence of archaeal amoA genes in terrestrial hot springs [J]. Environ Microbiol, 2008, 74 (20): 6417-6426
18 Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. Nitrification in terrestrial hot springs of Iceland and Kamchatka [J]. FEMS Microbiol Ecol, 2008, 64 (2): 167-174
19 Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring [J]. PNAS, 2008, 105 (6): 2134-2139
20 de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol [J]. Environ Microbiol, 2008, 10 (3): 810-818
21 Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Sinninghe Damste JS, Kim GJ, Madsen EL, Rhee SK. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil [J]. Environ Microbiol, 2011, 77 (24): 8635-8647
22 Kim JG, Jung MY, Park SJ, Rijpstra WI, Sinninghe Damste JS, Madsen EL, Min D, Kim JS, Kim GJ, Rhee SK. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil [J]. Environ Microbiol, 2012, 14 (6): 1528-1543
23 Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil [J]. PNAS, 2011, 108 (38): 15892-15897
24 Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Damste JSS. Archaeal nitrification in the ocean [J]. PNAS, 2006, 103 (33): 12317-12322
25 Santoro AE, Casciotti KL. Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation [J]. ISME J, 2011, 5 (11): 1796-1808
26 Matsutani N, Nakagawa T, Nakamura K, Takahashi R, Yoshihara K, Tokuyama T. Enrichment of a novel marine ammonia-oxidizing archaeon obtained from sand of an eelgrass zone [J]. Microbes Environ., 2011, 26 (1): 23-29
27 Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre [J]. Environ Microbiol, 2007, 9 (5): 1162-1175
28 Bai Y, Sun Q, Wen D, Tang X. Abundance of ammonia-oxidizing bacteria and archaea in industrial and domestic wastewater treatment systems [J]. FEMS Microbiol Ecol, 2012, 80 (2): 323-330
29 Zhang T, Jin T, Yan Q, Shao M, Wells G, Criddle C, HH PF. Occurrence of ammonia-oxidizing Archaea in activated sludges of a laboratory scale reactor and two wastewater treatment plants [J]. J Appl Microbiol, 2009, 107 (3): 970-977
30 Park HD, Wells GF, Bae H, Criddle CS, Francis CA. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors [J]. Environ Microbiol, 2006, 72 (8): 5643-5647
31 Wang S, Wang Y, Feng X, Zhai L, Zhu G. Quantitative analyses of ammonia-oxidizing Archaea and bacteria in the sediments of four nitrogen-rich wetlands in China [J]. Environ Microbiol,2011, 90 (2): 779-787
32 Sims A, Gajaraj S, Hu Z. Seasonal population changes of ammonia-oxidizing organisms and their relationship to water quality in a constructed wetland [J]. Ecol Eng, 2012, 40: 100-107
33 Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R, Hu ZQ. Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands [J]. Water Res, 2012, 46 (13): 4121-4129
34 Karner MB, DeLong EF, Karl DM. Archaeal dominance in the mesopelagic zone of the Pacific Ocean [J]. Nature, 2001, 409 (6819): 507-510
35 Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean [J]. PNAS, 2005, 102 (41): 14683-14688
36 Nakagawa T, Mori K, Kato C, Takahashi R, Tokuyama T. Distribution of cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea [J]. Microbes Environ, 2007, 22 (4): 365-372
37 Mosier, AC, Francis CA. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary [J]. Environ Microbiol, 2008, 10 (11): 3002-3016
38 Santoro AE, Francis CA, de Sieyes NR, Boehm AB. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary [J]. Environ Microbiol, 2008, 10 (4): 1068-1079
39 Cao H,Auguet JC, Gu JD. Global ecological pattern of ammonia-oxidizing archaea. PloS ONE, 2013, 8 (2): e52853
40 Auguet JC,Casamayor EO. A hotspot for cold crenarchaeota in the neuston of high mountain lakes [J]. Environ Microbiol, 2008, 10 (4): 1080-1086
41 Herrmann M, Saunders AM, Schramm A.Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments [J]. Appl Environ Microbiol, 2009, 75 (10): 3127-3136
42 Jiang HC, Dong HL, Yu BS, Lv G, Deng SC, Berzins N, Dai MH. Diversity and Abundance of Ammonia-Oxidizing Archaea and Bacteria in Qinghai Lake, Northwestern China [J]. Geomicrobiol J, 2009, 26 (3): 199-211
43 Auguet JC, Nomokonova N, Camarero L, Casamayor EO. Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in Oligotrophic Alpine Lakes [J]. Appl Environ Microbiol, 2011, 77 (6): 1937-1945
44 Hou J, Song CL, Cao XY, Zhou YY. Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu) [J]. Water Res, 2013, 47 (7): 2285-2296
45 Schleper C, Nicol GW. Ammonia-oxidising archaea—physiology, ecology and evolution [J]. Adv Microb Physiol, 2010, 57: 1-41
46 Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils [J]. Nature, 2006,442 (7104): 806-809
47 Nicol GW, Leininger S, Schlepe C, Prosser JI. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria [J]. Environ Microbiol, 2008, 10 (11): 2966-2978
48 Tourna M, Freitag TE, Nicol GW, Prosser JI. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms [J]. Environ Microbiol, 2008, 10 (5): 1357-1364
49 Lu L, Jia Z. Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environ Microbiol, 2013, 15 (6): 1795-1809
50 Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam [J]. Environ Microbiol, 2008, 10 (6): 1601-1611
51 贺纪正, 沈菊培, 张丽梅. 土壤中温泉古菌研究进展[J]. 生态学报, 2009, 29 (9): 5047-5055 [He JZ, Shen JP, Zhang LM. Advance in the research of soil non-thermophilic Crenarchaeota [J]. Acta Ecol Sin, 2009, 29 (9): 5047-5055]
52 Urakawa H, Tajima Y,Numata Y, Tsuneda S. Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems [J]. Appl Environ Microbiol, 2008, 74 (3): 894-900
53 Jin T, Zhang T, Yan Q. Characterization and quantification of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in a nitrogen-removing reactor using T-RFLP and qPCR [J]. Appl Environ Microbiol, 2010, 87 (3): 1167-1176
54 Kasuga I, Nakagaki H, Kurisu F, Furumai H. Predominance of ammonia-oxidizing archaea on granular activated carbon used in a full-scale advanced drinking water treatment plant [J]. Water Res, 2010, 44 (17): 5039-5049
55 Kayee P, Sonthiphand P, Rongsayamanont C, Limpiyakorn T. Archaeal amoA genes outnumber bacterial amoA genes in municipal wastewater treatment plants in Bangkok [J]. Microb Ecol, 2011, 62 (4): 776-788
56 Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polpraser C. Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants [J]. Bioresource Technol, 2011, 102 (4): 3694-3701
57 Mussmann M, Brito I, Pitcher A, Sinninghe Damste JS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Muller A, Daims H,Wagner M, Head IM. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers [J]. PNAS, 2011, 108 (40): 16771-16776
58 Yasuda T, Waki M, Kuroda K, Hanajima D, Fukumoto Y, Yamagishi T, Suwa Y, Suzuki K. Responses of community structure of amoA-encoding archaea and ammonia-oxidizing bacteria in ammonia biofilter with rockwool mixtures to the gradual increases in ammonium and nitrate [J]. J Appl Microbiol, 2013, 114 (3): 746-761
59 Hugoni M, Etien S, Bourges A, Lepere C, Domaizon I, Mallet C, Bronner G, Debroas D, Mary I. Dynamics of ammonia-oxidizing Archaea and Bacteria in contrasted freshwater ecosystems [J]. Res Microbiol, 2013, 164 (4): 360-370
60 Zhang T, Ye L, Tong AH, Shao MF, Lok S. Ammonia-oxidizing archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors [J]. Appl Environ Microbiol, 2011, 91 (4): 1215-1225
61 Gerhard WW, Marion DP, Friedrich WG, Wolfgang H, Stan-Lotter H. Communities of Archaea and Bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota [J]. Appl Environ Microbiol, 2007, 73 (1): 259-270
62 Sauder LA, Peterse F, Schouten S, Neufeld JD. Low-ammonia niche of ammonia-oxidizing archaea in rotating biological contactors of a municipal wastewater treatment plant [J]. Environ Microbiol, 2012, 14 (9): 2589-2600
63 Avrahami S, Jia Z, Neufeld JD, Murrell JC, Conrad R, Kusel K. Active autotrophic ammonia-oxidizing bacteria in biofilm enrichments from simulated creek ecosystems at two ammonium concentrations respond to temperature manipulation [J]. Appl Environ Microbiol, 2011, 77 (20): 7329-7338
64 Pratscher J, Dumont MG, Conrad R. Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil [J]. PNAS, 2011, 108 (10): 4170-4175
65 Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria [J]. Nature, 2009, 461 (7266): 976-979
66 Adair KL, Schwartz E. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA [J]. Microb Ecol, 2008, 56 (3): 420-426
67 Avrahami S, Liesack W, Conrad R. Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers [J]. Environ Microbiol, 2003, 5 (8): 691-705
68 Limpiyakorn T, Furhacker M, Haberl R, Chodanon T, Srithep P, Sonthiphand P. amoA-encoding archaea in wastewater treatment plants: a review [J]. Appl Environ Microbiol, 2013, 97 (4): 1425-1439
69 Herrmann M, Saunders AM, Schramm A. Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora [J]. Appl Environ Microbiol, 2008, 74 (10): 3279-3283
70 Chen, XP, Zhu YG, Xia Y, Shen JP, He JZ. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? [J]. Environ Microbiol, 2008, 10 (8): 1978-1987
71 He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H. 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 [J]. Environ Microbiol, 2007, 9 (9): 2364-2374
72 Bengtson P, Sterngren AE, Rousk J. Archaeal abundance across a pH gradient in an arable soil and its relationship to bacterial and fungal growth rates [J]. Appl Environ Microbiol, 2012, 78 (16): 5906-5911
73 Pereira ESMC, Poly F, Guillaumaud N, van Elsas JD, Salles JF. Fluctuations in ammonia oxidizing communities across agricultural soils are driven by soil structure and pH [J]. Front Microbiol, 2012, 3 (77): 1-22
74 Zhang LM, Hu HW, Shen JP, He JZ. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils [J]. ISME J, 2012, 6 (5): 1032-1045
75 Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea [J]. FEMS Microbiol Rev, 2009, 33 (5): 855-869
76 Oishi R, Tada C, Asano R, Yamamoto N, Suyama Y, Nakai Y. Growth of ammonia-oxidizing archaea and bacteria in cattle manure compost under various temperatures and ammonia concentrations [J]. Microb Ecol, 2012, 63 (4):787-793
77 Xie K, Jia X, Xu P, Huang X, Gu W, Zhang F, Yang S, Tang S. Improved composting of poultry feces via supplementation with ammonia oxidizing archaea [J]. Bioresource technol, 2012, 120: 70-77
78 Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil [J]. PNAS, 2011,108 (20) : 8420-8425

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