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How sequential reduction of terminal electron acceptors modulates nitrification and dynamics of nitrifying bacteria and archaea in a tropical vertisol

Published online by Cambridge University Press:  10 April 2018

Santosh Ranjan Mohanty ,
Rakhi Yadav ,
Garima Dubey ,
Usha Ahirwar ,
Neha Ahirwar ,
K. Aparna ,
D. L. N. Rao  and
Bharati Kollah
Santosh Ranjan Mohanty*
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
Rakhi Yadav
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
Garima Dubey
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
Usha Ahirwar
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
Neha Ahirwar
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
K. Aparna
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
D. L. N. Rao
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
Bharati Kollah
Affiliation:
ICAR - Indian Institute of Soil Science, Nabibagh, Bhopal, 462038, India
*
Author for correspondence: Santosh Ranjan Mohanty, E-mail: santosh.mohanty@icar.gov.in
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Abstract

Nitrification potential of a tropical vertisol saturated with water was estimated during sequential reduction of nitrate (NO3−), ferric iron (Fe3+), sulphate (SO42−) and carbon dioxide (CO2) in terminal electron-accepting processes (TEAPs). In general, the TEAPs enhanced potential nitrification rate (PNR) of the soil. Nitrification was highest at Fe3+ reduction followed by SO42− reduction, NO3− reduction and lowest in unreduced control soil. Predicted PNR correlated significantly with the observed PNR. Electron donor Fe2+ stimulated PNR, while S2− inhibited it significantly. Terminal-restriction fragment length polymorphism targeting the amoA gene of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) highlighted population dynamics during the sequential reduction of terminal electron acceptors. Only the relative abundance of AOA varied significantly during the course of soil reduction. Relative abundance of AOB correlated with NO3− and Fe2+. Linear regression models predicted PNR from the values of NO3−, Fe2+ and relative abundance of AOA. Principal component analysis of PNR during different reducing conditions explained 72.90% variance by PC1 and 19.52% variance by PC2. Results revealed that AOA might have a significant role in nitrification during reducing conditions in the tropical flooded ecosystem of a vertisol.

Keywords

ArchaeabacterianitrificationTEAPsvertisol
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 156 , Issue 2 , March 2018 , pp. 215 - 224
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Copyright
Copyright © Cambridge University Press 2018 

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References

Blaise, D, Amberger, A and von Tucher, S (1997) Influence of iron pyrites and dicyandiamide on nitrification and ammonia volatilization from urea applied to loess brown earths (luvisols). Biology and Fertility of Soils 24, 179–182.Google Scholar
Caffrey, JM (1995) Spatial and seasonal patterns in sediment nitrogen remineralization and ammonium concentrations in San Francisco Bay, California. Estuaries 18, 219–233.Google Scholar
Coleman, ML (1993) Microbial processes: controls on the shape and composition of carbonate concretions. Marine Geology 113, 127–140.Google Scholar
Davidson, EA and Janssens, IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173.Google Scholar
de Mendiburu, F (2014) Agricolae: Statistical Procedures for Agricultural Research. R Package Version 1.1-6. Lima Peru: The Comprehensive R Archive Network.Google Scholar
Elliott, P, Ragusa, S and Catcheside, D (1998) Growth of sulphate-reducing bacteria under acidic conditions in an upflow anaerobic bioreactor as a treatment system for acid mine drainage. Water Research 32, 3724–3730.Google Scholar
Flood, M, et al. (2015) Ammonia-oxidizing bacteria and archaea in sediments of the Gulf of Mexico. Environmental Technology 36, 124–135.Google Scholar
Francis, CA, et al. (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences USA 102, 14683–14688.Google Scholar
Froelich, PN, et al. (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochimica et Cosmochimica Acta 43, 1075–1090.Google Scholar
Gao, S, et al. (2002) Comparison of redox indicators in a paddy soil during rice-growing season. Soil Science Society of America Journal 66, 805–817.Google Scholar
Gribaldo, S, et al. (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature Reviews Microbiology 8, 743–752.Google Scholar
Horz, H-P, et al. (2000) Identification of major subgroups of ammonia-oxidizing bacteria in environmental samples by T-RFLP analysis of amoA PCR products. Journal of Microbiological Methods 39, 197–204.Google Scholar
Ihaka, R and Gentleman, R (1996) R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5, 299–314.Google Scholar
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 Microbiology Ecology 80, 193–203.Google Scholar
Jackson, ML (1958) Soil Chemical Analysis. Englewood, Cliffs, NJ: Prentice- Hall, Inc.Google Scholar
Joye, SB and Hollibaugh, JT (1995) Influence of sulphide inhibition of nitrification on nitrogen regeneration in sediments. Science 270, 623–625.Google Scholar
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. Applied and Environmental Microbiology 77, 8635–8647.Google Scholar
Kowalchuk, GA, et al. (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environmental Microbiology 2, 99–110.Google Scholar
Kox, MA and Jetten, MSM (2015) The nitrogen cycle. In Lugtenberg, B (ed.). Principles of Plant-Microbe Interactions. Berlin, Germany: Springer, pp. 205–214.Google Scholar
Kuenen, JG and Robertson, LA (1993) The use of natural bacterial populations for the treatment of sulphur-containing wastewater. In Rosenberg, E (ed.). Microorganisms to Combat Pollution. Dordrecht, The Netherlands: Springer, pp. 115–130.Google Scholar
Leininger, S, et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809.Google Scholar
Li, JJ, et al. (2014) Effects of groundwater geochemical constituents on degradation of benzene, toluene, ethylbenzene, and xylene coupled to microbial dissimilatory Fe (III) reduction. Environmental Engineering Science 31, 202–208.Google Scholar
Lovley, DR, et al. (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Archives of Microbiology 159, 336–344.Google Scholar
Matulewich, VA, Strom, PF and Finstein, MS (1975) Length of incubation for enumerating nitrifying bacteria present in various environments. Applied Microbiology 29, 265–268.Google Scholar
McCartney, DM and Oleszkiewicz, JA (1991) Sulphide inhibition of anaerobic degradation of lactate and acetate. Water Research 25, 203–209.Google Scholar
Mintie, AT, et al. (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Applied and Environmental Microbiology 69, 3129–3136.Google Scholar
Mohanty, SR, et al. (2014) Methane oxidation and methane driven redox process during sequential reduction of a flooded soil ecosystem. Annals of Microbiology 64, 65–74.Google Scholar
Moore, JN, Ficklin, WH and Johns, C (1988) Partitioning of arsenic and metals in reducing sulfidic sediments. Environmental Science and Technology 22, 432–437.Google Scholar
Oksanen, J, et al. (2007) The vegan Package. Community Ecology Package, version 1.8-8. Finland: The Comprehensive R Archive Network.Google Scholar
Park, H-D and Noguera, DR (2004) Evaluating the effect of dissolved oxygen on ammonia-oxidizing bacterial communities in activated sludge. Water Research 38, 3275–3286.Google Scholar
Patrick, WH and Delaune, RD (1972) Characterization of the oxidized and reduced zones in flooded soil. Soil Science Society of America Journal 36, 573–576.Google Scholar
Radax, R, et al. (2012) Ammonia-oxidizing archaea as main drivers of nitrification in cold-water sponges. Environmental Microbiology 14, 909–923.Google Scholar
Rittle, KA, Drever, JI and Colberg, PJS (1995) Precipitation of arsenic during bacterial sulphate reduction. Geomicrobiology Journal 13, 1–11.CrossRefGoogle Scholar
Schmidt, EL and Belser, LW (1982) Nitrifying bacteria. In Page, AL, Miller, RH and Keeney, DR (eds). Methods of Soil Analysis, Part2: Microbiological and Biochemical Properties Madison, WI: ASA, SSSA, pp. 1027–1042.Google Scholar
Searle, PL (1979) Measurement of adsorbed sulphate in soils – effects of varying soil: extractant ratios and methods of measurement. New Zealand Journal of Agricultural Research 22, 287–290.Google Scholar
Shyu, C, et al. (2007) MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. Microbial Ecology 53, 562–570.CrossRefGoogle ScholarPubMed
Siripong, S and Rittmann, BE (2007) Diversity study of nitrifying bacteria in full-scale municipal wastewater treatment plants. Water Research 41, 1110–1120.Google Scholar
Stookey, LL (1970) Ferrozine – a new spectrophotometric reagent for iron. Analytical Chemistry 42, 779–781.Google Scholar
Szukics, U, et al. (2012) Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiological Research 167, 103–109.Google Scholar
Tanji, KK, et al. (2003) Characterizing redox status of paddy soils with incorporated rice straw. Geoderma 114, 333–353.Google Scholar
Tourna, M, et al. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the United States of America 108, 8420–8425.Google Scholar
Treusch, AH, et al. (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environmental Microbiology 7, 1985–1995.Google Scholar
Walther, GR, et al. (2002) Ecological responses to recent climate change. Nature 416, 389–395.Google Scholar
Watson, SW, et al. (1986) Nitrospira marina gen. nov. sp. nov.: a chemolithotrophic nitrite-oxidizing bacterium. Archives of Microbiology 144, 1–7.Google Scholar
Yang, Y, et al. (2016) Ammonia-oxidizing archaea and bacteria in water columns and sediments of a highly eutrophic plateau freshwater lake. Environmental Science and Pollution Research International 23, 15358–15369.Google Scholar
Ying, J-Y, Zhang, L-M and He, J-Z (2010) Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environmental Microbiology Reports 2, 304–312.Google Scholar
Zhang, JZ and Millero, FJ (1994) Investigation of metal sulfide complexes in sea water using cathodic stripping square wave voltammetry. Analytica Chimica Acta 284, 497–504.Google Scholar
Zhou, M, Ye, H and Zhao, X (2014 a) Isolation and characterization of a novel heterotrophic nitrifying and aerobic denitrifying bacterium Pseudomonas stutzeri KTB for bioremediation of wastewater. Biotechnology and Bioprocess Engineering 19, 231–238.Google Scholar
Zhou, Z, et al. (2014 b) Inhibitory effects of sulfide on nitrifying biomass in the anaerobic–anoxic–aerobic wastewater treatment process. Journal of Chemical Technology and Biotechnology 89, 214–219.Google Scholar