Full Text:   <3832>

CLC number: Q938.1+3

On-line Access: 2012-06-29

Received: 2012-01-10

Revision Accepted: 2012-05-30

Crosschecked: 2012-09-06

Cited: 17

Clicked: 6396

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
1. Reference List
Open peer comments

Journal of Zhejiang University SCIENCE B 2012 Vol.13 No.10 P.769-782


Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary

Author(s):  Xiao-ran Li, Yi-ping Xiao, Wen-wei Ren, Zeng-fu Liu, Jin-huan Shi, Zhe-xue Quan

Affiliation(s):  Department of Microbiology and Microbial Engineering, School of Life Sciences, Fudan University, Shanghai 200433, China; more

Corresponding email(s):   quanzx@fudan.edu.cn

Key Words:  Wetland, Nitrification, Ammonia-oxidizing microorganisms, Abundance, Composition

Xiao-ran Li, Yi-ping Xiao, Wen-wei Ren, Zeng-fu Liu, Jin-huan Shi, Zhe-xue Quan. Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary[J]. Journal of Zhejiang University Science B, 2012, 13(10): 769-782.

@article{title="Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary",
author="Xiao-ran Li, Yi-ping Xiao, Wen-wei Ren, Zeng-fu Liu, Jin-huan Shi, Zhe-xue Quan",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary
%A Xiao-ran Li
%A Yi-ping Xiao
%A Wen-wei Ren
%A Zeng-fu Liu
%A Jin-huan Shi
%A Zhe-xue Quan
%J Journal of Zhejiang University SCIENCE B
%V 13
%N 10
%P 769-782
%@ 1673-1581
%D 2012
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1200013

T1 - Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary
A1 - Xiao-ran Li
A1 - Yi-ping Xiao
A1 - Wen-wei Ren
A1 - Zeng-fu Liu
A1 - Jin-huan Shi
A1 - Zhe-xue Quan
J0 - Journal of Zhejiang University Science B
VL - 13
IS - 10
SP - 769
EP - 782
%@ 1673-1581
Y1 - 2012
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1200013

Tidal flats are soil resources of great significance. nitrification plays a central role in the nitrogen cycle and is often a critical first step in nitrogen removal from estuarine and coastal environments. We determined the abundance as well as composition of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) in different soils during land reclamation process. The abundance of AOA was higher than that of AOB in farm land and wild land while AOA was not detected in tidal flats using real-time polymerase chain reaction (PCR). The different abundances of AOB and AOA were negatively correlated with the salinity. The diversities of AOB and AOA were also investigated using clone libraries by amplification of amoA gene. Among AOB, nearly all sequences belonged to the Nitrosomonas lineage in the initial land reclamation process, i.e., tidal flats, while both Nitrosomonas and Nitrosospira lineages were detected in later and transition phases of land reclamation process, farm land and wild land. The ratio of the numbers of sequences of Nitrosomonas and Nitrosospira lineages was positively correlated with the salinity and the net nitrification rate. As for AOA, there was no obvious correlation with the changes in the physicochemical properties of the soil. This study suggests that AOB may be more import than AOA with respect to influencing the different land reclamation process stages.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Allen, J.G., Beutel, M.W., Call, D.R., Fischer, A.M., 2010. Effects of oxygenation on ammonia oxidation potential and microbial diversity in sediment from surface-flow wetland mesocosms. Bioresour. Technol., 101(4):1389-1392.

[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(10):6152-6164.

[3]Avrahami, S., Conrad, R., Braker, G., 2002. Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl. Environ. Microbiol., 68(11):5685-5692.

[4]Bastida, F., Zsolnay, A., Hernandez, T., Garcia, C., 2008. Past, present and future of soil quality indices: a biological perspective. Geoderma, 147(3-4):159-171.

[5]Bastien, P., Procop, G.W., Reischl, U., 2008. Quantitative real-time PCR is not more sensitive than “conventional” PCR. J. Clin. Microbiol., 46(6):1897-1900.

[6]Bernhard, A.E., Bollmann, A., 2010. Estuarine nitrifiers: new player, patterns and processes. Estuar. Coast. Shelf Sci., 88(1):1-11.

[7]Bernhard, A.E., Donn, T., Giblin, A.E., Stahl, D.A., 2005. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ. Microbiol., 7(9):1289-1297.

[8]Bernhard, A.E., Tucker, J., Giblin, A.E., Stahl, D.A., 2007. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ. Microbiol., 9(6):1439-1447.

[9]Boatman, C.D., Murray, J.W., 1982. Modeling exchangeable NH4+ adsorption in marine sediments: process and controls of adsorption. Limnol. Oceanogr., 27(1):99-110.

[10]Boyle-Yarwood, S.A., Bottomley, P.J., Myrold, D.D., 2008. Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ. Microbiol., 10(11):2956-2965.

[11]Boynton, W.R., Kemp, W.M., 1985. Nutrient regeneration and oxygen consumption by sediments along an estuarine salinity gradient. Mar. Ecol. Prog. Ser., 23:45-55.

[12]Brochier-Armanet, C., Boussau, B., Gribaldo, S., Forterre, P., 2008. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol., 6(3):245-252.

[13]Charette, M.A., Buesseler, K.O., 2004. Submarine groundwater discharge of nutrients and copper to an urban subestuary of Chesapeake Bay (Elizabeth River). Limnol. Oceanogr., 49(2):376-385.

[14]Chen, X.P., Zhu, Y.G., Xia, Y., Shen, J.P., He, J.Z., 2008. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol., 10(8):1978-1987.

[15]Chu, H.Y., Fujii, T., Morimoto, S., Lin, X.G., Yagi, K., Hu, J.L., Zhang, J.B., 2007. Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Appl. Environ. Microbiol., 73(2):485-491.

[16]Dang, H.Y., Li, J., Chen, R.P., Wang, L., Guo, L.Z., Zhang, Z.N., Klotz, M.G., 2010. Diversity, abundance, and spatial distribution of sediment ammonia-oxidizing betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China. Appl. Environ. Microbiol., 76(14):4691-4702.

[17]Di, H.J., Cameron, K.C., Shen, J.P., Winefield, C.S., O′Callaghan, M., Bowatte, S., He, J.Z., 2010. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol., 72(3):386-394.

[18]Dorador, C., Busekow, A., Vila, I., Imhoff, J.F., Witzel, K.P., 2008. Molecular analysis of enrichment cultures of ammonia oxidizers from the Salar de Huasco, a high altitude saline wetland in northern Chile. Extremophiles, 12(3):405-414.

[19]Enwall, K., Philippot, L., Hallin, S., 2005. Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl. Environ. Microbiol., 71(12):8335-8343.

[20]Fernandez, I.J., Simmons, J.A., Briggs, R.D., 2000. Indices of forest floor nitrogen status along a climate gradient in Maine, USA. For. Ecol. Manage., 134(1-3):177-187.

[21]Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. PNAS, 103(3):626-631.

[22]Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E., Oakley, B.B., 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. PNAS, 102(41):14683-14688.

[23]Gan, X.J., Cai, Y.T., Choi, C.Y., Ma, Z.J., Chen, J.K., Li, B., 2009. Potential impacts of invasive Spartina alterniflora on spring bird communities at Chongming Dongtan, a Chinese wetland of international importance. Estuar. Coast. Shelf Sci., 83(2):211-218.

[24]Gao, Y., Zhao, B., 2006. The effect of reclamation on mud flat development in Chongming Island, Shanghai. Chin. Agric. Sci. Bull., 22(8):475-479 (in Chinese).

[25]Girvan, M.S., Bullimore, J., Pretty, J.N., Osborn, A.M., Ball, A.S., 2003. Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl. Environ. Microbiol., 69(3):1800-1809.

[26]Good, I.J., 1953. The population frequencies of species and the estimation of population parameters. Biometrika, 40(3-4):237-264.

[27]Hafez, H.M., Hauck, R., Lüschow, D., McDougald, L., 2005. Comparison of the specificity and sensitivity of PCR, nested PCR, and real-time PCR for the diagnosis of histomoniasis. Avian Dis., 49(3):366-370.

[28]Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic. Acids Symp. Ser., 41:95-98.

[29]He, J.Z., Shen, J.P., Zhang, L.M., Zhu, Y.G., Zheng, Y.M., Xu, M.G., 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(9):2364-2374.

[30]Head, I.M., Hiorns, W.D., Embley, T.M., McCarthy, A.J., Saunders, J.R., 1993. The phylogeny of autotrophic ammonia-oxdizing bacteria as determined by analysis of 16S ribosomal-RNA gene-sequences. Microbiology, 139(6):1147-1153.

[31]Ibekwe, A.M., Grieve, C.M., Lyon, S.R., 2003. Characterization of microbial communities and composition in constructed dairy wetland wastewater effluent. Appl. Environ. Microbiol., 69(9):5060-5069.

[32]Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., Gibson, T.J., 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci., 23(10):403-405.

[33]Jia, Z.J., Conrad, R., 2009. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol., 11(7):1658-1671.

[34]Kelly, C.N., Schoenholtz, S.H., Adams, M.B., 2011. Soil properties associated with net nitrification following watershed conversion from Appalachian hardwoods to Norway spruce. Plant Soil, 344(1-2):361-376.

[35]Könneke, M., Bernhard, A., de la Torre, J., Walker, C., Waterbury, J., Stahl, D., 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437(7058):543-546.

[36]Kowalchuk, G.A., Stienstra, A.W., Heilig, G.H.J., Stephen, J.R., Woldendorp, J.W., 2000. Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ. Microbiol., 2(1):99-110.

[37]Kumar, S., Tamura, K., Nei, M., 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinformatics, 5(2):150-163.

[38]Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Schuster, S.C., Schleper, C., 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 442(7104):806-809.

[39]Li, X., Zhou, Y.X., Kuang, R.Y., 2010. Analysis and trend prediction of shoreline evolution in Chongming Dongtan, Shanghai. J. Jilin Univ., 40:417-424 (in Chinese).

[40]Mertens, J., Broos, K., Wakelin, S.A., Kowalchuk, G.A., Springael, D., Smolders, E., 2009. Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J., 3(8):916-923.

[41]Moin, N.S., Nelson, K.A., Bush, A., Bernhard, A.E., 2009. Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl. Environ. Microbiol., 75(23):7461-7468.

[42]Norman, R.J., Stucki, J.W., 1981. The determination of nitrate and nitrite in soil extracts by ultraviolet spectrophotometry. Soil Sci. Soc. Am. J., 45(2):347-353.

[43]Park, H.D., Wells, G.F., Bae, H., Criddle, C.S., Francis, C.A., 2006. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol., 72(8):5643-5647.

[44]Paul, E.A., Clark, F.E., 1989. Soil Microbiology and Biochemistry. Academic Press, San Diego.

[45]Purkhold, U., Pommerening-Röser, A., Juretschko, S., Schmid, M.C., 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.

[46]Purkhold, U., Wagner, M., Timmermann, G., Pommerening-Roser, A., Koops, H.P., 2003. 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int. J. Syst. Evol. Microbiol., 53(5):1485-1494.

[47]Rhoades, C.C., Coleman, D.C., 1999. Nitrogen mineralization and nitrification following land conversion in montane Ecuador. Soil Biol. Biochem., 31(10):1347-1354.

[48]Rotthauwe, J.H., Witzel, K.P., 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(12):4704-4712.

[49]Rysgaard, S., Thastum, P., Dalsgaard, T., Christensen, P.B., Sloth, N.P., 1999. Effects of salinity on NH4+ adsorption capacity, nitrification, and dentrification in Danish estuarine sediments. Estuaries, 22(1):21-30.

[50]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(2):175-186.

[51]Santoro, A.E., Francis, C.A., de Sieyes, N.R., Boehm, A.B., 2008. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ. Microbiol., 10(4):1068-1079.

[52]Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al., 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol., 75(23):7537-7541.

[53]Sharp, J., Pennock, J., Church, T., Tramontano, J., Cifuentes, L., 1984. The Estuarine Interaction of Nutrients, Organics, and Metals: A Case Study in the Delaware Estuary. In: Kennedy, V.S. (Ed.), The Estuary as a Filter. Academic Press, New York, p.241-258.

[54]Shen, J.P., Zhang, L.M., Zhu, Y.G., Zhang, J.B., He, J.Z., 2008. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol., 10(6):1601-1611.

[55]Solorzano, L., 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr., 14(5):799-801.

[56]Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D.A., Wagner, M., Schleper, C., 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol., 18(8):331-340.

[57]Treusch, A.H., Leininger, S., Kletzin, A., Schuster, S.C., Klenk, H.P., 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(12):1985-1995.

[58]Venter, J., Remington, K., Heidelberg, J., Halpern, A., Rusch, D., Eisen, J., Wu, D., Paulsen, I., Nelson, K., Nelson, W., et al., 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304(5667):66-74.

[59]Wang, Y.A., Ke, X.B., Wu, L.Q., Lu, Y.H., 2009. Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Syst. Appl. Microbiol., 32(1):27-36.

[60]Ward, B.B., O′Mullan, G.D., 2002. Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing gamma-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl. Environ. Microbiol., 68(8):4153-4157.

[61]Ward, B.B., Evelllard, D., Klrshteln, J.D., Nelson, J.D., Voytek, M.A., Jackson, G.A., 2007. Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray. Environ. Microbiol., 9(10):2522-2538.

[62]Wells, G.F., Park, H.D., Yeung, C.H., Eggleston, B., Francis, C.A., Criddle, C.S., 2009. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ. Microbiol., 11(9):2310-2328.

[63]Windom, H., Niencheski, F., 2003. Biogeochemical processes in a freshwater-seawater mixing zone in permeable sediments along the coast of Southern Brazil. Mar. Chem., 83(3-4):121-130.

[64]Zhang, L.M., Wang, M., Prosser, J.I., Zheng, Y.M., He, J.Z., 2009. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol., 70(2):208-217.

[65]Zhang, L.M., Offre, P.R., He, J.Z., Verhamme, D.T., Nicol, G.W., Prosser, J.I., 2010. Autotrophic ammonia oxidation by soil thaumarchaea. PNAS, 107(40):17240-17245.

[66]Zhou, J., Bruns, M.A., Tiedje, J.M., 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol., 62(2):316-322.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2024 Journal of Zhejiang University-SCIENCE