Abundance and distribution of ammonia-oxidizing archaea in Tibetan and Yunnan plateau agricultural soils of China

Abstract

As low oxygen and high ultraviolet (UV) exposure might significantly affect the microbial existence in plateau, it could lead to a specialized microbial community. To determine the abundance and distribution of ammonia-oxidizing archaea (AOA) in agricultural soil of plateau, seven soil samples were collected respectively from farmlands in Tibet and Yunnan cultivating the wheat, highland-barley, and colza, which are located at altitudes of 3200–3800 m above sea level. Quantitative PCR (q-PCR) and clone library targeting on amoA gene were used to quantify the abundances of AOA and ammonia-oxidizing bacteria (AOB), and characterize the community structures of AOA in the samples. The number of AOA cells (9.34 × 10⁷–2.32 × 10⁸ g^-1 soil) was 3.86–21.84 times greater than that of AOB cells (6.91 × 10⁶–1.24 × 10⁸ g^-1 soil) in most of the samples, except a soil sample cultivating highland-barley with an AOA/AOB ratio of 0.90. Based Kendall’s correlation coefficient, no remarkable correlation between AOA abundance and the environmental factor was observed. Additionally, the diversities of AOA community were affected by total nitrogen and organic matter concentration in soils, suggesting that AOA was probably sensitive to several environmental factors, and could adjust its community structure to adapt to the environmental variation while maintaining its abundance.

Keywords

ammonia-oxidizing archaea / ammonia-oxidizing bacteria / quantitative PCR / clone library / plateau

References

[1] WagnerM, RathG, AmannR, KoopsH P, SchleiferK H. In-situ identification of ammonia-oxidizing bacteria. Systematic and Applied Microbiology, 1995, 18(2): 251–264

[2] BockE, WagnerM. Oxidation of inorganic nitrogen compounds as an energy source. In: DworkinM, FalkowS, RosenbergE, SchleiferK H, StackebrandtE, editors. The Prokaryotes-An Evolving Electronic Resource for the Microbiological Community. 3rd ed. New York: Springer, 2001, 457–495

[3] HallamS J, MincerT J, SchleperC, PrestonC M, RobertsK, RichardsonP M, DeLongE F. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biology, 2006, 4(4): 520–536

[4] KönnekeM, BernhardA E, de la TorreJ R, WalkerC B, WaterburyJ B, StahlD A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 2005, 437(7058): 543–546

[5] HatzenpichlerR, LebedevaE V, SpieckE, StoeckerK, RichterA, DaimsH, WagnerM. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(6): 2134–2139

[6] ParkB J, ParkS J, YoonD N, SchoutenS, Sinninghe DamstéJ S, RheeS K. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Applied and Environmental Microbiology, 2010, 76(22): 7575–7587

[7] MatsutaniN, NakagawaT, NakamuraK, TakahashiR, YoshiharaK, TokuyamaT. Enrichment of a novel marine ammonia-oxidizing archaeon obtained from sand of an eelgrass zone. Microbes Environ, 2011, 26(1): 23–29

[8] TournaM, StieglmeierM, SpangA, KönnekeM, SchintlmeisterA, UrichT, EngelM, SchloterM, WagnerM, RichterA, SchleperC. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(20): 8420–8425

[9] LeiningerS, UrichT, SchloterM, SchwarkL, QiJ, NicolG W, ProsserJ I, SchusterS C, SchleperC. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 2006, 442(7104): 806–809

[10] MosierA C, FrancisC A. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environmental Microbiology, 2008, 10(11): 3002–3016

[11] AgoguéH, BrinkM, DinasquetJ, HerndlG J. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature, 2008, 456(7223): 788–791

[12] KasugaI, NakagakiH, KurisuF, FurumaiH. Predominance of ammonia-oxidizing archaea on granular activated carbon used in a full-scale advanced drinking water treatment plant. Water Research, 2010, 44(17 17SI): 5039–5049

[13] ParkH D, WellsG F, BaeH, CriddleC S, FrancisC A. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Applied and Environmental Microbiology, 2006, 72(8): 5643–5647

[14] LimpiyakornT, SonthiphandP, RongsayamanontC, PolprasertC. Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresource Technology, 2011, 102(4): 3694–3701

[15] WuchterC, AbbasB, CoolenM J, HerfortL, van BleijswijkJ, TimmersP, StrousM, TeiraE, HerndlG J, MiddelburgJ J, SchoutenS, Sinninghe DamstéJ S. Archaeal nitrification in the ocean. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33): 12317–12322

[16] MussmannM, BritoI, PitcherA, Sinninghe DamstéJ S, HatzenpichlerR, RichterA, NielsenJ L, NielsenP H, MüllerA, DaimsH, WagnerM, HeadI M. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(40): 16771–16776

[17] NicolG W, LeiningerS, SchleperC, ProsserJ I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology, 2008, 10(11): 2966–2978

[18] ZhangL M, WangM, ProsserJ I, ZhengY M, HeJ Z. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiology Ecology, 2009, 70(2): 208–217

[19] DiH J, CameronK C, ShenJ P, WinefieldC S, O’CallaghanM, BowatteS, HeJ Z. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience, 2009, 2(9): 621–624

[20] VerhammeD T, ProsserJ I, NicolG W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. The ISME journal, 2011, 5(6): 1067–1071

[21] SchaussK, FocksA, LeiningerS, KotzerkeA, HeuerH, Thiele-BruhnS, SharmaS, WilkeB M, MatthiesM, SmallaK, MunchJ C, AmelungW, KaupenjohannM, SchloterM, SchleperC. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environmental Microbiology, 2009, 11(2): 446–456

[22] ZhaoZ Q, LiS C, GaoJ B, WangY L. Identifying spatial patterns and dynamics of climate change using recurrence quantification analysis: a case study of qinghai-tibet plateau. International Journal of Bifurcation and Chaos in Applied Sciences and Engineering, 2011, 21(04): 1127–1139

[23] XuX K, ChenH, LevyJ K. Spatiotemporal vegetation cover variations in the Qinghai-Tibet Plateau under global climate change. Chinese Science Bulletin, 2008, 53(6): 915–922

[24] XuZ H, ChenC R, HeJ Z, LiuJ X. Trends and challenges in soil research 2009: linking global climate change to local long-term forest productivity. Journal of Soils and Sediments, 2009, 9(2): 83–88

[25] FrancisC A, RobertsK J, BemanJ M, SantoroA E, OakleyB B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(41): 14683–14688

[26] RotthauweJ H, WitzelK P, LiesackW. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology, 1997, 63(12): 4704–4712

[27] HeJ Z, ShenJ P, ZhangL M, ZhuY G, ZhengY M, XuM G, DiH J. 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. Environmental Microbiology, 2007, 9(9): 2364–2374

[28] Gubry-RanginC, NicolG W, ProsserJ I. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiology Ecology, 2010, 74(3): 566–574

[29] MertensB, BoonN, VerstraeteW. Stereospecific effect of hexachlorocyclohexane on activity and structure of soil methanotrophic communities. Environmental Microbiology, 2005, 7(5): 660–669

[30] WittebolleL, VervaerenH, VerstraeteW, BoonN. Quantifying community dynamics of nitrifiers in functionally stable reactors. Applied and Environmental Microbiology, 2008, 74(1): 286–293

[31] JuretschkoS, TimmermannG, SchmidM, SchleiferK H, Pommerening-RöserA, KoopsH P, WagnerM. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Applied and Environmental Microbiology, 1998, 64(8): 3042–3051

[32] AdairK L, SchwartzE. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microbial Ecology, 2008, 56(3): 420–426

[33] SteinL Y, ArpD J. Loss of ammonia monooxygenase activity in nitrosomonas europaea upon exposure to nitrite. Applied and Environmental Microbiology, 1998, 64(10): 4098–4102

[34] WangX, WenX, CriddleC, YanH, ZhangY, DingK. Bacterial community dynamics in two full-scale wastewater treatment systems with functional stability. Journal of Applied Microbiology, 2010, 109(4): 1218–1226

[35] SuzukiM T, GiovannoniS J. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology, 1996, 62(2): 625–630

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 51078207), and Research Fund for the Doctoral Program of High Education of China (No. 20090002770003). We wish to thank the staff of Research Platform for Modern Environmental Biologic Technology of School of Environment in Tsinghua University.

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg