Ecological niche differentiation of ammonia-oxidising archaea and bacteria in acidic soils due to land use change
Shenyan Dai A , Qian Liu A , Jun Zhao A E and Jinbo Zhang B C D E
+ Author Affiliations
- Author Affiliations
A School of Geography Sciences, Nanjing Normal University, Nanjing 210023, China.
B Key Laboratory of Virtual Geographical Environment (Nanjing Normal University), Ministry of Education, Nanjing, 210023, China.
C State Key Laboratory Cultivation Base of Geographical Environment Evolution (Jiangsu Province), Nanjing, 210023, China.
D Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, 210023, China.
E Corresponding author. Email: junzhao37@126.com; zhangjinbo@njnu.edu.cn
Soil Research 56(1) 71-79 https://doi.org/10.1071/SR16356
Submitted: 14 December 2016 Accepted: 7 July 2017 Published: 4 September 2017
Abstract
Nitrification can be driven by either ammonia-oxidising bacteria (AOB) or ammonia-oxidising archaea (AOA) and is a central process in the nitrogen cycle. However, to date, it is not clear how the ecological niche differentiation of AOB and AOA are affected by land use and management changes in strongly acidic soils in subtropical China. In this study, three different land-use acidic soils – forest, upland, and paddy soils – were collected and a DNA Stable-Isotope Probing experiment performed to determine the relative contributions of AOA and AOB to ammonia oxidation in these soils. The results showed that AOA, but not AOB, amoA genes were detected in 13C-labelled DNA in the forest and paddy soils; however, only AOB amoA genes were detected in 13C-labelled DNA in the upland agricultural soils. The growth and activity of AOA and AOB in the different land-use soils provided direct evidence for the shift in roles for AOA and AOB in ammonia oxidation. AOA played the predominant role in ammonia oxidation in acidic forest and paddy soils. However, AOB, not AOA, mainly regulated the ammonia oxidation in acidic upland agricultural soils. Phylogenetic analysis indicated that AOA members within the marine Group1.1a-associated lineage dominated nitrification in the forest and paddy soils. Ammonia oxidation in the upland soil was catalysed by Nitrosospira cluster 3-like AOB. The moisture condition was likely the main reason inducing the ecological niche differentiation between upland and paddy soils; and AOA was more suitable for growth in the flooded, low oxygen conditions.
Additional keywords: ammonia oxidation, DNA Stable-Isotope Probing experiment, forest soil, paddy soil, upland soil.
References
Adair K, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in soils along an elevation gradient in northern Arizona, USA. Microbial Ecology 56, 420–426.| Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in soils along an elevation gradient in northern Arizona, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOntrzM&md5=18061dfb643576dcd5a5042860a06c53CAS |
Alawi M, Off S, Kaya M, Spieck E (2009) Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge. Environmental Microbiology Reports 1, 184–190.
| Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlaltr4%3D&md5=220798a82a34402c9cd495b00e8c3cefCAS |
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. Applied and Environmental Microbiology 68, 5685–5692.
| Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1ajsbY%3D&md5=1651a901e399794722ee6855c5638149CAS |
Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. The ISME Journal 2, 429–441.
| Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvVGrtbc%3D&md5=7df40930520a4333826d50b45a2da856CAS |
Chu HY, Morimoto S, Fujii T, Yagi K (2009) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Science Society of America Journal 73, 2026–2031.
| Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSku7jK&md5=48c45c16e102cb63cb81072234072b1cCAS |
Coolen MJL, Abbas B, Van Bleijswijk J, Hopmans EC, Kuypers MMM, Wakeham SG (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. Environmental Microbiology 9, 1001–1016.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlOrtLk%3D&md5=9d6224bbec98dfe53a148dca6a6d86c7CAS |
De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biology & Biochemistry 33, 853–866.
| Nitrification in acid soils: micro-organisms and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVOrtb8%3D&md5=f4d087c32508179ab2d074118b948f6aCAS |
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S (2009) Nitrification driven by bacteria and not archaea in nitrogen rich grassland soils. Nature Geoscience 2, 621–624.
| Nitrification driven by bacteria and not archaea in nitrogen rich grassland soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKktLbE&md5=5553eec0484d4a7cbfc76d684bf121a8CAS |
Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology Reviews 33, 855–869.
| Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWksbnE&md5=d2a0c4a8e02c805ad8e1bf3966da5878CAS |
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 103, 626–631.
| The diversity and biogeography of soil bacterial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOiurY%3D&md5=9cd0bf37b35ecf2a92c6473accf56bebCAS |
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. Proceedings of the National Academy of Sciences of the United States of America 102, 14683–14688.
| Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKjsb7J&md5=fa18c68cc96040f2a713386ec9c8eaebCAS |
Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiology Ecology 74, 566–574.
| Archaea rather than bacteria control nitrification in two agricultural acidic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFKmsrvO&md5=4cc6e1abd787c4bc1e15c7cdab4e951eCAS |
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PW, Zhang FS (2010) Significant acidification in major Chinese croplands. Proceedings of the National Academy of Sciences of the United States of America 327, 1008–1010.
Hai B, Diallo NH, Sall D, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Much JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystem. Applied and Environmental Microbiology 75, 4993–5000.
| Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSgtrvM&md5=7c13988ad416bca66dd3b113ad5df0ceCAS |
Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America 105, 2134–2139.
| A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitl2ls7o%3D&md5=79f9228b218629d2711498a24fa71d29CAS |
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG (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. Environmental Microbiology 9, 2364–2374.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVyku7rE&md5=dfc04e163d6986aea8b462f9ca14657bCAS |
Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 11, 1658–1671.
| Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlyhurs%3D&md5=e26afb95c1fa959ad92291cb71d71de5CAS |
Kirkham D, Bartholomew WV (1954) Equations for following nutrient transformations in soil, utilizing tracer data 1. Soil Science Society of America Journal 18, 33–34.
| Equations for following nutrient transformations in soil, utilizing tracer data 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXjslSmsA%3D%3D&md5=c65f0b191329ac788dc70f70e17e8000CAS |
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Review of Microbiology 55, 485–529.
| Ammonia-oxidizing bacteria: a model for molecular microbial ecology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslKjtLs%3D&md5=f69c9a7f7734871ad993d3887741086cCAS |
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=c1befa57a1ec3a7d167061a421506f64CAS |
Lehtovirta LE, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota. FEMS Microbiology Ecology 70, 367–376.
| Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaqsLnN&md5=3cb2eeb67a739fdbd67c0a7c143b05faCAS |
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809.
| Archaea predominate among ammonia-oxidizing prokaryotes in soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFKmtrs%3D&md5=d40895be20de1ef73de01620f3864cdaCAS |
Lu RK (2000) ‘Soil agro-chemical analyses.’ (Agricultural Technical Press of China: Beijing) [in Chinese]
Lu L, Jia Z (2013) Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environmental Microbiology 15, 1795–1809.
| Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOjsbo%3D&md5=5d6a9578f5a73fd5e17d713a7b0b9322CAS |
Lu L, Han W, Zhang J, Wu Y, Wang B, Lin X (2012) Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea. The ISME Journal 6, 1978–1984.
| Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtlynt7rO&md5=990153b77582357c8e8daacb433a19bfCAS |
Lueders T, Manefield M, Friedrich MW (2004) Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environmental Microbiology 6, 73–78.
| Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Sntbg%3D&md5=892518d999c3b028fe9095250d61c33cCAS |
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.
| Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtF2kurrL&md5=4c8310bd36c33f6d72865f174cafd8f3CAS |
Mendum TA, Sockett RE, Hirsch PR (1999) Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the subdivision of the class Proteobacteria in arable soils to nitrogen fertilizer. Applied and Environmental Microbiology 65, 4155–4162.
Nicol GW, 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. Environmental Microbiology 10, 2966–2978.
| The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGitrnF&md5=4cb855742b34ea1c29c70fdb3da12f7dCAS |
Offre P, Prosser JI, Nicol GW (2009) Growth of ammonia oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiology Ecology 70, 99–108.
| Growth of ammonia oxidizing archaea in soil microcosms is inhibited by acetylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgsr3L&md5=47cb694215abd25f4d121e48b90fcc73CAS |
Oved T, Shaviv A, Goldrath T, Mandelbaum RT, Minz D (2001) Influence of effluent irrigation on community composition and function of ammonia-oxidizing bacteria in soil. Applied and Environmental Microbiology 67, 3426–3433.
| Influence of effluent irrigation on community composition and function of ammonia-oxidizing bacteria in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFSltbs%3D&md5=f31427b851179d9a07e48951c8f5915cCAS |
Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environmental Microbiology 10, 2931–2941.
| Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGitrnK&md5=f4e7402c19cc7671959322046895a734CAS |
Revsbech NP, Pedersen O, Reichardt W, Briones A (1999) Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions. Biology and Fertility of Soils 29, 379–385.
| Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions.Crossref | GoogleScholarGoogle Scholar |
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. Applied and Environmental Microbiology 63, 4704–4712.
Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology 10, 1068–1079.
| Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVentbo%3D&md5=7b9d9b3ac83ebfbc40f1affe281a71e7CAS |
Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology 10, 1601–1611.
| Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVWkurk%3D&md5=f89ed5c48743279146e05f705c7b530aCAS |
Stephen JR, Kowalchuk GA, Bruns MAV, McCaig AE, Phillips CJ, Embley TM, Prosser JI (1998) Analysis of b-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Applied and Environmental Microbiology 64, 2958–2965.
Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environmental Microbiology 10, 1357–1364.
| Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtFyhtro%3D&md5=77d1c71cf1567dd7d007639fca149022CAS |
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. The ISME Journal 5, 1067–1071.
| Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtF2hsrg%3D&md5=9c4d084d4bc83b0d6173b3ac08a5193eCAS |
Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of beta-proteobacterial ammonia oxidizer populations. Applied and Environmental Microbiology 68, 20–30.
| Grassland management regimens reduce small-scale heterogeneity and species diversity of beta-proteobacterial ammonia oxidizer populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Wiuw%3D%3D&md5=aa32ab05217706b4972dea8b01f7bc0eCAS |
Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P (2006) Archaeal nitrification in the ocean. Proceedings of the National Academy of Sciences of the United States of America 103, 12317–12322.
| Archaeal nitrification in the ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1Klsbg%3D&md5=6a99686517c90025a97d9c4fc88e748aCAS |
Xia W, Zhang C, Zeng X, Feng Y, Weng J, Lin X (2011) Autotrophic growth of nitrifying community in an agricultural soil. The ISME Journal 5, 1226–1236.
| Autotrophic growth of nitrifying community in an agricultural soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVaqsLs%3D&md5=0edc1ba38fb080151399f048ae3c5c46CAS |
Xu YB, Cai ZC (2007) Denitrification characteristics of subtropical soils in China affected by soil parent material and land use. European Journal of Soil Science 58, 1293–1303.
| Denitrification characteristics of subtropical soils in China affected by soil parent material and land use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVWmuw%3D%3D&md5=f3be5665c2f69428b709c5b9c72b62d7CAS |
Xun WB, Xiong W, Huang T, Ran W, Li DC, Shen QR, Li Q, Zhang RF (2016) Swine manure and quicklime have different impacts on chemical properties and composition of bacterial communities of an acidic soil. Applied Soil Ecology 100, 38–44.
| Swine manure and quicklime have different impacts on chemical properties and composition of bacterial communities of an acidic soil.Crossref | GoogleScholarGoogle Scholar |
Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proceedings of the National Academy of Sciences of the United States of America 107, 17240–17245.
| Autotrophic ammonia oxidation by soil thaumarchaea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSjurvI&md5=2e32350f7e48cdc5a37c6ef42fcf0f48CAS |
Zhang JB, Zhu TB, Cai ZC, Müller C (2011) Nitrogen cycling in forest soils across climate gradients in Eastern China. Plant and Soil 342, 419–432.
| Nitrogen cycling in forest soils across climate gradients in Eastern China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslKksLs%3D&md5=b03235ad86f821624b02ce339a70ed36CAS |
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. The ISME Journal 6, 1032–1045.
| Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVGktrw%3D&md5=0a27d54b8df373beaf5648e1446d7a57CAS |
Zhang JB, Cai ZC, Zhu TB, Yang WY, Müller C (2013a) Mechanisms for the retention of inorganic N in acidic forest soils of southern China. Scientific Reports 3, 2342
| Mechanisms for the retention of inorganic N in acidic forest soils of southern China.Crossref | GoogleScholarGoogle Scholar |
Zhang JB, Zhu T, Meng T, Zhang Y, Yang J, Yang W, Müller C, Cai ZC (2013b) Agricultural land use affects nitrate production and conservation in humid subtropical soils in China. Soil Biology & Biochemistry 62, 107–114.
| Agricultural land use affects nitrate production and conservation in humid subtropical soils in China.Crossref | GoogleScholarGoogle Scholar |
Zhao J, Ni T, Li J, Lu Q, Fang ZY, Huang QW, Zhang RF, Li R, Shen B, Shen QR (2016) Effects of organic-inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice-wheat cropping system. Applied Soil Ecology 99, 1–12.
| Effects of organic-inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice-wheat cropping system.Crossref | GoogleScholarGoogle Scholar |
Zhu HH, Chen C, Xu C, Zhu QH, Huang DY (2016) Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environmental Pollution 219, 99–106.
| Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslGrtbfE&md5=b3ddd7c32a1e4655694152cb11c23511CAS |
