Abstract
Ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) play an important role in the oxidation of ammonia. The diversity and relative abundance of AOA and AOB in compost samples from four composting stages [initial (day 0), heating (day 3), thermophilic (day 12), and cooling (day 28) stage ] were analyzed using the amoA gene as a functional marker. The number of operational taxonomic units (OTUs) found in each stage during sewage sludge composting was 33.3 % to 66.6 % of the total OTUs for AOB and 43.8 % to 62.5 % for AOA, with OTUs defined on the basis of a 5 % difference in nucleotides. Phylogenetic analysis showed that the AOB amoA sequences related to the Nitrosomonas lineage were dominant throughout the entire composting process. Most of the AOA amoA sequences fell into a soil/sediment cluster containing “Candidatus Nitrososphaera gargensis”. These results indicate that different ammonia oxidizers were present in different stages during composting, but that the dominant phylogenetic types were stable.
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Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari. Mexico Appl Environ Microbiol 72(12):7767–7777
Brown MN, Briones A, Diana J, Raskin L (2013) Ammonia-oxidizing archaea and nitrite-oxidizing nitrospiras in the biofilter of a shrimp recirculating aquaculture system. FEMS Microbiol Ecol 83(1):17–25
Burrell PC, Phalen CM, Hovanec TA (2001) Identification of bacteria responsible for ammonia oxidation in freshwater aquaria. Appl Environ Microbiol 67(12):5791–5800
Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1(7):660–662
Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil. Environ Microbiol 10(8):1978–1987
De La Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10(3):810–818
Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister‐Boltenstern S, Sessitsch A (2010) Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74(3):575–591
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 U S A 105(6):2134–2139
Huang GF, Wong JWC, Wu QT, Nagar BB (2004) Effect of C/N on composting of pig manure with sawdust. Waste Manage 24(8):805–813
Innerebner G, Knapp B, Vasara T, Romantschuk M, Insam H (2006) Traceability of ammonia-oxidizing bacteria in compost-treated soils. Soil Biol Biochem 38(5):1092–1100
Keluskar R, Desai A (2014) Evaluation of hydroxylamine oxidoreductase as a functional and phylogenetic marker to differentiate Nitrosomonas spp. J Basic Microbiol 54(4):261–268
Kosobucki P, Chmarzynski A, Buszewski B (2000) Sewage sludge composting. Pol J Environ Stud 9(4):243–248
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55(1):485–529
Kowalchuk GA, Naoumenko ZS, Derikx PJL, Felske A, Stephen JR, Arkhipchenko IA (1999) Molecular analysis of ammonia-oxidizing bacteria of the β subdivision of the class Proteobacteria in compost and composted materials. Appl Environ Microbiol 65(2):396–403
Li R, Wang JJ, Zhang Z, Shen F, Zhang G, Qin R, Li X, Xiao R (2012) Nutrient transformations during composting of pig manure with bentonite. Bioresour Technol 121:362–368
Li Y, Li W, Liu B, Wang K, Su C, Wu C (2013) Ammonia emissions and biodegradation of organic carbon during sewage sludge composting with different extra carbon sources. Int Biodeterior Biodegrad 85:624–630
Park H-D, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72(8):5643–5647
Satisha GC, Devarajan L (2007) Effect of amendments on windrow composting of sugar industry pressmud. Waste Manage 27(9):1083–1091
Sauder LA, Engel K, Stearns JC, Masella AP, Pawliszyn R, Neufeld JD (2011) Aquarium nitrification revisited: Thaumarchaeota are the dominant ammonia oxidizers in freshwater aquarium biofilters. PLoS One 6(8):e23281
Singh RP, Singh P, Ibrahim MH, Hashim R (2011) Land application of sewage sludge: physicochemical and microbial response. Rev Environ Contam Toxicol 214:41–61
Siripong S, Rittmann BE (2007) Diversity study of nitrifying bacteria in full-scale municipal wastewater treatment plants. Water Res 41(5):1110–1120
Sonthiphand P, Limpiyakorn T (2011) Change in ammonia-oxidizing microorganisms in enriched nitrifying activated sludge. Appl Microbiol Biotechnol 89(3):843–853
Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101
Wang X, Wang W, Gao L, Cui Z (2006) Protocols of applification of denaturing gradient gel electrophoresis (DGGE) in studies of environmental microorganism. J China Agric Univ 11(5):1–7
Wei Y-S, Fan Y-B, Wang M-J (2001) A cost analysis of sewage sludge composting for small and mid-scale municipal wastewater treatment plants. Resour Conserv Recy 33(3):203–216
Yamada T, Araki S, Ikeda-Ohtsubo W, Okamura K, Hiraishi A, Ueda H, Ueda Y, Miyauchi K, Endo G (2013) Community structure and population dynamics of ammonia oxidizers in composting processes of ammonia-rich livestock waste. Syst Appl Microbiol 36(5):359–367
Yamamoto N, Otawa K, Nakai Y (2010) Diversity and abundance of ammonia-oxidizing bacteria and ammonia-oxidizing archaea during cattle manure composting. Microb Ecol 60(4):807–815
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(4):1501–1510
Zeng G, Zhang J, Chen Y, Yu Z, Yu M, Li H, Liu Z, Chen M, Lu L, Hu C (2011) Relative contributions of archaea and bacteria to microbial ammonia oxidation differ under different conditions during agricultural waste composting. Bioresour Technol 102(19):9026–9032
Zeng Y, De Guardia A, Ziebal C, De Macedo FJ, Dabert P (2013) Impact of biodegradation of organic matters on ammonia oxidation in compost. Bioresour Technol 136:49–57
Zhang T, Ye L, Tong AHY, Shao M-F, Lok S (2011) Ammonia-oxidizing archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors. Appl Microbiol Biotechnol 91(4):1215–1225
Zhu S, Chan G, Cai KL, Qu LH, Huang LN (2007) Leachates from municipal solid waste disposal sites harbor similar, novel nitrogen-cycling bacterial communities. FEMS Microbiol Lett 267(2):236–242
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31270536), Key Projects in the National Science & Technology Pillar Program during the Twelfth Five-Year Plan Period (Grant No. 2012BAD12B05-3), Program of Science and Technology Innovation Team Building in Heilongjiang Province (2012TD006), and Key Science and Technology Program of Heilongjiang Province (GC12B306).
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Yan, L., Li, Z., Bao, J. et al. Diversity of ammonia-oxidizing bacteria and ammonia-oxidizing archaea during composting of municipal sludge. Ann Microbiol 65, 1729–1739 (2015). https://doi.org/10.1007/s13213-014-1012-y
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DOI: https://doi.org/10.1007/s13213-014-1012-y