Abstract
Dynamics of ammonia-oxidizing bacterial (AOB) and archaeal (AOA) abundance was assayed in a tropical Humic Nitisol during two cropping seasons of a long-term field experiment situated in the central highlands of Kenya. Since 2002, soils were treated yearly with biochemically contrasting organic inputs (4 Mg C ha−1 year−1) of Tithonia diversifolia (TD; C/N ratio: 13; lignin: 8.9 %; polyphenols: 1.7 %), Calliandra calothyrsus (CC; 13; 13; 9.4) and Zea mays (ZM; 59; 5.4; 1.2) combined with and without 120 kg CaNH4NO3 ha−1 season−1. In 2012 and 2013, soils (0–15 cm) were sampled at young growth (EC30) and flowering (EC60) stages of maize and subjected to DNA-based amoA gene quantification. ZM and TD increased AOB abundance by 9 and 19 %, respectively, compared to CC, while AOA remained unaffected. This was ascribed to high organic N in TD and lower lignin and polyphenol contents in ZM than in CC. In CC, formation of polyphenol-protein complexes limited microbial access to N. Sole use of mineral N or its combination with organic inputs decreased AOA abundance by 35 % but not AOB as a consequence of pH reduction by mineral N. Overall, AOB was more responsive than AOA to input quality that became most pronounced under optimal soil moisture conditions found in 2013 and at EC60 in 2012. We recommend prolonged study periods, considering also rRNA-based analyses to explore the dynamics of active nitrifying communities as a consequence of interrelations of contrasting organic inputs, crop growth stages and seasonality in agricultural soils.
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References
Avrahami S, Bohannan BJM (2007) Response of Nitrosospira sp. strain AF-Like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173
Chivenge P, Vanlauwe B, Gentile R, Wangechi H, Mugendi D, van Kessel C, Six J (2009) Organic and mineral input management to enhance crop productivity in central Kenya. Agron J 101:1266–1275
Chivenge P, Vanlauwe B, Gentile R, Six J (2011) Organic resource quality influences short-term aggregate dynamics and soil organic carbon and nitrogen accumulation. Soil Biol Biochem 43:657–666
Cray JA, Russell JT, Timson DJ, Singhal RS, Hallsworth JE (2013) A universal measure of chaotropicity and kosmotropicity: a universal measure of chao- and kosmotropicity. Environ Microbiol 15:287–296
Cray JA, Stevenson A, Ball P, Bankar SB, Eleutherio ECA, Ezeji TC, Singhal RS, Thevelein JM, Timson DJ, Hallsworth JE (2015) Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Curr Opin Biotechnol 33:228–259
de Gannes V, Eudoxie G, Hickey WJ (2014) Impacts of edaphic factors on communities of ammonia-oxidizing archaea, ammonia-oxidizing bacteria and nitrification in tropical soils. PLoS ONE 9:1–14
de Lima Alves F, Stevenson A, Baxter E, Gillion JLM, Hejazi F, Hayes S, Morrison IEG, Prior BA, McGenity TJ, Rangel DEN, Magan N, Timmis KN, Hallsworth JE (2015) Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window. Curr Genet 61:457–477
Jones A, Breuning-Madsen H, Deckers J, Dewitte, O, Gallali T, Le Roux P, Micheli E, Montanarella L, Spaargaren O, Thiombiano L, van Ranst E, Yemefack M, Zougmore R (2013) Soil atlas of Africa. http://eusoils.jrc.ec.europa.eu/library/maps/africa_atlas/
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions: ammonia-oxidizing bacteria and archaea. FEMS Microbiol Ecol 72:386–394
España M, Rasche F, Kandeler E, Brune T, Rodriguez B, Bending GD, Cadisch G (2011) Identification of active bacteria involved in decomposition of complex maize and soybean residues in a tropical vertisol using 15 N-DNA stable isotope probing. Pedobiologia 54:187–193
FAO (2006) World reference base for soil resources. FAO, Rome
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. Proc Natl Acad Sci USA 102:14683–14688
Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms—a review. Soil Biol Biochem 75:54–63
Gentile R, Vanlauwe B, van Kessel C, Six J (2009) Managing N availability and losses by combining fertilizer-N with different quality residues in Kenya. Agric Ecosyst Environ 131:308–314
Gentile R, Vanlauwe B, Kavoo A, Chivenge P, Six J (2011a) Residue quality and N fertilizer do not influence aggregate stabilization of C and N in two tropical soils with contrasting texture. Nutr Cycl Agroecosyst 88:121–131
Gentile R, Vanlauwe B, Six J (2011b) Litter quality impacts short-but not long-term soil carbon dynamics in soil aggregate fractions. Ecol Appl 21:695–703
Gleeson DB, Müller C, Banerjee S, Ma W, Siciliano SD, Murphy DV (2010) Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Biol Biochem 42:1888–1891
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
Hai B, Dialo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000
Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605
Hallsworth JE, Heim S, Timmis KN (2003) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5:1270–1280
Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci 105:2134–2139
He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, 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 9:2364–2374
Hepburn JS (1908) The modifications of the Kjeldahl method for the quantitative determination of nitrogen. Franklin Institute 166:81–89
ICRAF (1999) Laboratory methods for soil and plant analysis. International Centre for Research in Agroforestry, Nairobi
Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
Kamolmanit B, Vityakon P, Kaewpradit W, Cadisch G, Rasche F (2013) Soil fungal communities and enzyme activities in a sandy, highly weathered tropical soil treated with biochemically contrasting organic inputs. Biol Fertil Soils 49:905–917
Kunlanit B, Vityakon P, Puttaso A, Cadisch G, Rasche F (2014) Mechanisms controlling soil organic carbon composition pertaining to microbial decomposition of biochemically contrasting organic residues: evidence from midDRIFTS peak area analysis. Soil Biol Biochem 76:100–108
Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt A, Goodfello M (eds) Nucleic acid techniques systematics, 1st edn. Wiley, West Sussex, pp 115–257
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Levičnik-Höfferle Š, Nicol GW, Ausec L, Mandic-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
Liu DL, Helyar KR, Conyers MK, Fisher R, Poile GJ (2004) Response of wheat, triticale and barley to lime application in semi-arid soils. Field Crops Res 90:287–301
Lueders T, Friedrich M (2000) Archaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66:2732–2742
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
Millar N, Baggs EM (2004) Chemical composition, or quality, of agroforestry residues influences N2O emissions after their addition to soil. Soil Biol Biochem 36:935–943
Milling A, Smalla K, Maidl FX, Schloter M, Munch JC (2005) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266:23–39
Morimoto S, Hayatsu M, Takada Hoshino Y et al (2011) Quantitative analyses of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in fields with different Soil Types. Microbes Environ 26:248–253
Muema EK, Cadisch G, Röhl C, Vanlauwe B, Rasche F (2015) Response of ammonia-oxidizing bacteria and archaea to biochemical quality of organic inputs combined with mineral nitrogen fertilizer in an arable soil. Appl Soil Ecol 95:128–139
Musyoki MK, Cadisch G, Enowashu E, Zimmermann J, Muema EK, Beed F, Rasche F (2015) Promoting effect of Fusarium oxysporum [f.sp. strigae] on abundance of nitrifying prokaryotes in a maize rhizosphere across soil types. Biol Control 83:37–45
Mutabaruka R, Hairiah K, Cadisch G (2007) Microbial degradation of hydrolysable and condensed tannin polyphenol–protein complexes in soils from different land-use histories. Soil Biol Biochem 39:1479–1492
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
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. Environ Microbiol 10:2966–2978
Onwonga RN, Lelei JJ, Mochoge BB (2010) Mineral nitrogen and microbial biomass dynamics under different acid soil management practices for maize production. J Agric Sci 2:16–30
Palm CA, Gachengo CN, Delve RJ, Cadisch G, Giller KE (2001a) Organic inputs for soil fertility management in tropical agroecosystems: application of an organic resource database. Agric Ecosyst Environ 83:27–42
Palm CA, Giller KE, Mafongoya PL, Swift MJ (2001b) Management of organic matter in the tropics: translating theory into practice. Nutr Cycl Agroecosyst 61:63–75
Partey ST, Preziosi RF, Robson GD (2013) Maize residue interaction with high quality organic materials: effects on decomposition and nutrient release dynamics. Agric Res 2:58–67
Piepho H-P (2009) Data transformation in statistical analysis of field trials with changing treatment variance. Agron J 101:865–869
Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–2941
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531
Rasche F, Cadisch G (2013) The molecular microbial perspective of organic matter turnover and nutrient cycling in tropical agroecosystems—What do we know? Biol Fertil Soils 49:251–262
Rasche F, Knapp D, Kaiser C, Koranda M, Kitzler B, Zechmeister-Boltenstern S, Richter A, Sessitsch A (2011) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402
Rasche F, Musyoki MK, Röhl C, Muema EK, Vanlauwe B, Cadisch G (2014) Lasting influence of biochemically contrasting organic inputs on abundance and community structure of total and proteolytic bacteria in tropical soils. Soil Biol Biochem 74:204–213
Rotthauwe JH, Witzel KP, 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
Sądej W, Przekwas K (2008) Fluctuations of nitrogen levels in soil profile under conditions of a long-term fertilization experiment. Plant Soil Environ 54:197–203
SAS Institute (2014) SAS system for windows, Version 9.4. SAS Institute Inc, Cary
Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke BM, Matthies M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456
Schleper C (2010) Ammonia oxidation: different niches for bacteria and archaea? ISME J 4:1092–1094
Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488
Schmidt MA, Kreinberg AJ, Gonzalez JM, Halvorson JJ, French E, Bollmann A, Hagerman AE (2013) Soil microbial communities respond differently to three chemically defined polyphenols. Plant Physiol Biochem 72:190–197
Schulz E (2004) Influence of site conditions and management on different soil organic matter (som) pools. Arch Agron Soil Sci 50:33–47
Schulz E, Körschens M (1998) Characterization of the decomposable part of soil organic matter (SOM) and transformation processes by hot water extraction. Eurasian Soil Sci 31:809–813
Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–221
Stevenson A, Hallsworth JE (2014) Water and temperature relations of soil Actinobacteria: water and temperature relations of Actinobacteria. Environ Microbiol Rep 6:744–755
Stevenson A, Cray JA, Williams JP, Santos R, Sahay R, Neuenkirchen N, McClure CD, Grant IR, Houghton JDR, Quinn JP, Timson DJ, Patil SV, Singhal RS, Anton J, Dijksterhuis J, Hocking AD, Lieven B, Rangel DEN, Voytek MA, Gunde-Cimerman N, Oren A, Timmis KN, McGenity TJ, Hallsworth JE (2015) Is there a common water-activity limit for the three domains of life? ISME J 9:1333–1351
Stopnišek N, Gubry-Rangin C, Höfferle Š, 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
Strauss SL, Reardon CL, Mazzola M (2014) The response of ammonia-oxidizer activity and community structure to fertilizer amendment of orchard soils. Soil Biol Biochem 68:410–418
Szukics U, Abell GCJ, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil: nitrifier and denitrifier response to a changing environment. FEMS Microbiol Ecol 72:395–406
Talbot JM, Finzi AC (2012) Litter decay rates are determined by lignin chemistry. Biogeochemistry 108:279–295
Valentine D (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323
Wessén E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45:193–200
Zhalnina K, Dörr de Quadros P, Camargo AO, Triplett EW (2012) Drivers of archaeal ammonia-oxidizing communities in soil. Terr Microbiol 3:1–9
Zhang LM, Offre PR, He JZ, Verhamme DT, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci 107:17240–17245
Zhang X, Liu W, Schloter M, Zhang G, Chen Q, Huang J, Li L, Elser JJ, Han X (2013) Response of the abundance of key soil microbial nitrogen-cycling genes to multi-factorial global changes. PLoS ONE 8:1–10
Acknowledgments
Scholarship support for the first author, field operations and laboratory expenses were financed by German Academic Exchange Service (DAAD) with funds of the Federal Ministry of Economic Cooperation and Development (BMZ) of Germany and by the foundation fiat panis Foundation (Ulm, Germany) through the Food Security Centre (FSC) of the University of Hohenheim (Germany). The authors thank Carolin Röhl for her technical support during the molecular analyses at University of Hohenheim. We are also grateful to Evonne Oyugi and the technical staff at CIAT (Nairobi, Kenya) for their support in soil analyses, and the field technicians Kiragu and Mureithi for soil samplings at the field experimental site. Special thanks go to Professor Dr. Hans-Peter Piepho, Dr. Joseph Ogutu and Dr. Juan Carlos Bayas Laso (Department of Bioinformatics, University of Hohenheim) for their support in statistical analysis.
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Muema, E.K., Cadisch, G., Musyoki, M.K. et al. Dynamics of bacterial and archaeal amoA gene abundance after additions of organic inputs combined with mineral nitrogen to an agricultural soil. Nutr Cycl Agroecosyst 104, 143–158 (2016). https://doi.org/10.1007/s10705-016-9762-5
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DOI: https://doi.org/10.1007/s10705-016-9762-5