Abstract
In addition to ammonia-oxidizing bacteria (AOB) the more recently discovered ammonia-oxidizing archaea (AOA) can also oxidize ammonia, but little is known about AOA community structure and abundance in subtropical forest soils. In this study, both AOA and AOB were investigated with molecular techniques in eight types of forests at surface soils (0–2 cm) and deep layers (18–20 cm) in Nanling National Nature Reserve in subtropical China. The results showed that the forest soils, all acidic (pH 4.24–5.10), harbored a wide range of AOA phylotypes, including the genera Nitrosotalea, Nitrososphaera, and another 6 clusters, one of which was reported for the first time. For AOB, only members of Nitrosospira were retrieved. Moreover, the abundance of the ammonia monooxygenase gene (amoA) from AOA dominated over AOB in most soil samples (13/16). Soil depth, rather than forest type, was an important factor shaping the community structure of AOA and AOB. The distribution patterns of AOA and AOB in soil layers were reversed: AOA diversity and abundances in the deep layers were higher than those in the surface layers; on the contrary, AOB diversity and abundances in the deep layers were lower than those in the surface layers. Interestingly, the diversity of AOA was positively correlated with pH, but negatively correlated with organic carbon, total nitrogen and total phosphorus, and the abundance of AOA was negatively correlated with available phosphorus. Our results demonstrated that AOA and AOB were differentially distributed in acidic soils in subtropical forests and affected differently by soil characteristics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agogue H, Brink M, Dinasquet J, Herndl GJ (2008) Major gradients in putatively nitrifying and non-nitrifying archaea in the deep North Atlantic. Nature 456:788–791
Alonso-Sáez L et al (2012) Role for urea in nitrification by polar marine archaea. Proc Natl Acad Sci USA 109:17989–17994. doi:10.1073/pnas.1201914109
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Alves RJE, Wanek W, Zappe A, Richter A, Svenning MM, Schleper C, Urich T (2013) Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea. ISME J 7:1620–1631. doi:10.1038/ismej.2013.35
Auguet J-C, Nomokonova N, Camarero L, Casamayor EO (2011) Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic Alpine lakes. Appl Environ Microbiol 77:1937–1945. doi:10.1128/aem.01213-10
Auguet J-C, Triado-Margarit X, Nomokonova N, Camarero L, Casamayor EO (2012) Vertical segregation and phylogenetic characterization of ammonia-oxidizing archaea in a deep oligotrophic lake. ISME J 6:1786–1797. doi:10.1038/ismej.2012.33
Beam JP, Jay ZJ, Kozubal MA, Inskeep WP (2014) Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park. ISME J 8:938–951. doi:10.1038/ismej.2013.193
Bertagnolli AD, Meinhardt KA, Pannu M, Brown S, Strand S, Fransen SC, Stahl DA (2015) Influence of edaphic and management factors on the diversity and abundance of ammonia-oxidizing Thaumarchaeota and bacteria in soils of bioenergy crop cultivars. Environ Microbiol Rep 7:312–320. doi:10.1111/1758-2229.12250
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Micro 6:245–252. doi:10.1038/nrmicro1852
Chen Z-M (2012) Ecosystem functions in Nanling National Nature Reserve and protective measures concerned. Shaanxi For Sci Technol 61–63:019
De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33:853–866. doi:10.1016/s0038-0717(00)00247-9
Dodsworth JA, Hungate BA, Hedlund BP (2011) Ammonia oxidation, denitrification and dissimilatory nitrate reduction to ammonium in two US Great Basin hot springs with abundant ammonia-oxidizing archaea. Environ Microbiol 13:2371–2386. doi:10.1111/j.1462-2920.2011.02508.x
Elser JJ et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
Fang YT, Gundersen P, Mo JM, Zhu WX (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352. doi:10.5194/bg-5-339-2008
FAOSTAT (2011) <http://faostat.fao.org/>
FDGP (2014) <http://www.gdf.gov.cn/>
Francis CA, Roberts KJ, Beman JM, Alyson ES, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688
Friedrich MW, Schmitt-Wagner D, Lueders T, Brune A (2001) Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil-feeding termite Cubitermes orthognathus. Appl Environ Microbiol 67:4880–4890. doi:10.1128/aem.67.10.4880-4890.2001
Goecks J, Nekrutenko A, Taylor J, Team TG (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86
Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574. doi:10.1111/j.1574-6941.2010.00971.x
Gubry-Rangin C et al (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA 108:21206–21211. doi:10.1073/pnas.1109000108
Hernández M, Dumont MG, Calabi M, Basualto D, Conrad R (2014) Ammonia oxidizers are pioneer microorganisms in the colonization of new acidic volcanic soils from South of Chile. Environ Microbiol Rep 6:70–79. doi:10.1111/1758-2229.12109
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. doi:10.1111/j.1462-2920.2012.02882.x
Hou E, Chen C, Wen D, Liu X (2015) Phosphatase activity in relation to key litter and soil properties in mature subtropical forests in China. Sci Total Environ 515–516:83–91
Isobe K et al (2012) High abundance of ammonia-oxidizing archaea in acidified subtropical forest soils in southern China after long-term N deposition. FEMS Microbiol Ecol 80:193–203
Jiang Y, Jin C, Sun B (2014) Soil aggregate stratification of nematodes and ammonia oxidizers affects nitrification in an acid soil. Environ Microbiol 16:3083–3094. doi:10.1111/1462-2920.12339
Jung M-Y et al (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal Group I.1a from an agricultural soil. Appl Environ Microbiol 77:8635–8647. doi:10.1128/aem.05787-11
Ke X, Angel R, Lu Y, Conrad R (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15:2275–2292. doi:10.1111/1462-2920.12098
Könneke M, Bernhard AE, Torre JRDL, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546
Koper TE, Stark JM, Habteselassie MY, Norton JM (2010) Nitrification exhibits Haldane kinetics in an agricultural soil treated with ammonium sulfate or dairy-waste compost. FEMS Microbiol Ecol 74:316–322. doi:10.1111/j.1574-6941.2010.00960.x
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529. doi:10.1146/annurev.micro.55.1.485
Lee K-H, Wang Y-F, Li H, Gu J-D (2014a) Niche specificity of ammonia oxidizing communities in a freshwater interior city wetland receiving municipal wastewater in Daqing, Northeast China. Ecotoxicology 23:2081–2091. doi:10.1007/s10646-014-1334-3
Lee K-H, Wang Y-F, Zhang G-X, Gu J-D (2014b) Distribution patterns of ammonia-oxidizing bacteria and anammox bacteria in the freshwater marsh of Honghe wetland in Northeast China. Ecotoxicology 23:1930–1942. doi:10.1007/s10646-014-1333-4
Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA 108:15892–15897. doi:10.1073/pnas.1107196108
Leininger S et al (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Levičnik-Höfferle Š, Nicol GW, Ausec L, Mandić-Mulec I, Prosser JI (2012) Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol Ecol 80:114–123. doi:10.1111/j.1574-6941.2011.01275.x
Lu R (2000) Methods of agriculture chemical analysis. China Agriculture Scientech Press, Beijing
Lu L et al (2012) Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea. ISME J 6:1978–1984
Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–979. doi:10.1038/nature08465
Nicol G, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978
NNNR (2015) <http://www.gdnl.org/>
Porder S, Asner GP, Vitousek PM (2005) Ground-based and remotely sensed nutrient availability across a tropical landscape. Proc Natl Acad Sci USA 102:10909–10912. doi:10.1073/pnas.0504929102
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531. doi:10.1016/j.tim.2012.08.001
Qin H et al (2013) Ammonia-oxidizing archaea are more important than ammonia-oxidizing bacteria in nitrification and NO3 −-N loss in acidic soil of sloped land. Biol Fertility Soils 49:767–776. doi:10.1007/s00374-012-0767-1
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
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. doi:10.1111/j.1462-2920.2012.02786.x
Schleper C (2010) Ammonia oxidation: different niches for bacteria and archaea? ISME J 4:1092–1094
Schleper C, Nicol GW (2010) Ammonia-oxidising archaea—physiology, ecology and evolution. In: Robert KP (ed) Advances in microbial physiology, vol 57. Academic Press, Oxford, pp 1–41. doi:10.1016/b978-0-12-381045-8.00001-1
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506. doi:10.1128/aem.71.3.1501-1506.2005
Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101. doi:10.1146/annurev-micro-092611-150128
Stopnisek N, Gubry-Rangin C, Hofferle S, Nicol GW, Mandic-Mulec I, Prosser JI (2010) Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment. Appl Environ Microbiol 76:7626–7634. doi:10.1128/aem.00595-10
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
Tourna M et al (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425. doi:10.1073/pnas.1013488108
Tripathi BM, Kim M, Lai-Hoe A, Shukor NAA, Rahim RA, Go R, Adams JM (2013) pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiol Ecol 86:303–311. doi:10.1111/1574-6941.12163
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071. doi:10.1038/ismej.2010.191
Wang Y-F, Gu J-D (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97:7015–7033. doi:10.1007/s00253-012-4430-4
Wang Y-F, Gu J-D (2014) Effects of allylthiourea, salinity and pH on ammonia/ammonium-oxidizing prokaryotes in mangrove sediment incubated in laboratory microcosms. Appl Microbiol Biotechnol 98:3257–3274. doi:10.1007/s00253-013-5399-3
Wang Y-F, Feng Y-Y, Ma X, Gu J-D (2013) Seasonal dynamics of ammonia/ammonium-oxidizing prokaryotes in oxic and anoxic wetland sediments of subtropical coastal mangrove. Appl Microbiol Biotechnol 97:7919–7934. doi:10.1007/s00253-012-4510-5
Wang Y-F, Li X-Y, Gu J-D (2014) Differential responses of ammonia/ammonium-oxidizing prokaryotes in mangrove sediment to amendment of acetate and leaf litter. Appl Microbiol Biotechnol 98:3165–3180. doi:10.1007/s00253-013-5318-7
Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513. doi:10.1126/science.1098778
Wessén E et al (2011) Spatial distribution of ammonia-oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISME J 5:1213–1225. doi:10.1038/ismej.2010.206
Winogradsky S (1890) Investigations on nitrifying organisms. Ann Inst Pasteur 4:213–321
Yamamoto N, Asano R, Yoshii H, Otawa K, Nakai Y (2011) Archaeal community dynamics and detection of ammonia-oxidizing archaea during composting of cattle manure using culture-independent DNA analysis. Appl Microbiol Biotechnol 90:1501–1510
Yao H et al (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625. doi:10.1128/aem.00136-11
Zhang L-M, Wang M, Prosser JI, Zheng Y-M, He J-Z (2009) Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol Ecol 70:208–217. doi:10.1111/j.1574-6941.2009.00775.x
Zhang L-M, Hu H-W, Shen J-P, He J-Z (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045
Zhang J-B, Cai Z-C, Zhu T-B, Yang W-Y, Müller C (2013) Mechanisms for the retention of inorganic N in acidic forest soils of southern China. Sci Rep 3:2342. doi:10.1038/srep02342
Zheng M, Huang J, Chen H, Wang H, Mo J (2015) Responses of soil acid phosphatase and beta-glucosidase to nitrogen and phosphorus addition in two subtropical forests in southern China. Eur J Soil Biol 68:77–84. doi:10.1016/j.ejsobi.2015.03.010
Zhou Z, Shi X, Zheng Y, Qin Z, Xie D, Li Z, Guo T (2014) Abundance and community structure of ammonia-oxidizing bacteria and archaea in purple soil under long-term fertilization. Eur J Soil Biol 60:24–33
Acknowledgments
This research was supported by a research grant to Yong-Feng Wang from National Natural Science Foundation of China [31470562] and fund to Guangdong Nanling Forest Ecology Station from The National Forestry Bureau of China. We would like to thank Mr. Sanwu Zhang for support in field sampling and Ms. Kelly Lau at The University of Hong Kong for general laboratory support in this research work. We are grateful to the editor and the reviewers for their careful revisions and constructive suggestions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Xian-Hua Gan and Fang-Qiu Zhang have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gan, XH., Zhang, FQ., Gu, JD. et al. Differential distribution patterns of ammonia-oxidizing archaea and bacteria in acidic soils of Nanling National Nature Reserve forests in subtropical China. Antonie van Leeuwenhoek 109, 237–251 (2016). https://doi.org/10.1007/s10482-015-0627-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-015-0627-8