Abstract
Ammonia oxidation is performed by both ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). Few studies compared the adaptability of AOA and AOB for oxygenated/hypoxic alternant conditions in water-level-fluctuating zones. Here, using qPCR and 454 high-throughput sequencing of functional amoA genes of AOA and AOB, we examined the changes of abundances, diversities, and community structures of AOA and AOB in periodically flooded soils compared to the non-flooded soils in Three Gorges Reservoir. The increased AOA operational taxonomic unit (OTU) numbers and the higher ratios of abundance (AOA:AOB) in the periodically flooded soils suggested AOA have better adaptability for oxygenated/hypoxic alternant conditions in the water-level-fluctuating zones in the Three Gorges Reservoir and probably responsible for the ammonia oxidation there. Canonical correspondence analysis (CCA) showed that oxidation-reduction potential (ORP) had the most significant effect on the community distribution of AOA (p < 0.01). Pearson analysis also indicated that ORP was the most important factor influencing the abundances and diversities of ammonia-oxidizing microbes. ORP was significantly negatively correlated with AOA OTU numbers (p < 0.05), ratio of OTU numbers (AOA:AOB) (p < 0.01), and ratio of amoA gene abundances (AOA:AOB) (p < 0.05). ORP was also significantly positively correlated with AOB abundance (p < 0.05).





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2:429–441
Blainey PC, Mosier AC, Potanina A, Francis CA and Quake SR (2011) Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6: e16626
Bock ESI, Stuven R, Zart D (1995) Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron donors and nitrite as electron acceptor. Arch Microbiol 163:16–20
Dang H, Luan XW, Chen R, Zhang X, Guo L, Klotz MG (2010) Diversity, abundance and distribution of amoA-encoding archaea in deep-sea methane seep sediments of the Okhotsk Sea. FEMS Microbiol Ecol 72:370–385
de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818
Fang F, Yang Y, Guo J, Zhou H, Fu C, Li Z (2011) Three-dimensional fluorescence spectral characterization of soil dissolved organic matters in the fluctuating water-level zone of Kai County, Three Gorges Reservoir. Front Environ Sci Eng China 5:426–434
Gorman-Lewis D, Martens-Habbena W, Stahl DA (2014) Thermodynamic characterization of proton-ionizable functional groups on the cell surfaces of ammonia-oxidizing bacteria and archaea. Geobiology 12:157–171
Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108:21206–21211
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 105:2134–2139
Hu BL, Shen LD, Liu S, Cai C, Chen TT, Kartal B, Harhangi HR, Op den Camp HJ, Lou LP, Xu XY, Zheng P, Jetten MS (2013) Enrichment of an anammox bacterial community from a flooded paddy soil. Environ Microbiol Rep 5:483–489
Hu BL, Liu S, Wang W, Shen LD, Lou LP, Liu WP, Tian GM, Xu XY, Zheng P (2014a) pH-dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. FEMS Microbiol Ecol 90:290–299
Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, He ZF, Geng S, Cheng DQ, Lou LP, Xu XY, Zheng P, He YF (2014b) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc Natl Acad Sci U S A 111:4495–4500
Jiang H, Huang Q, Dong H, Wang P, Wang F, Li W, Zhang C (2010) RNA-based investigation of ammonia-oxidizing archaea in hot springs of Yunnan Province, China. Appl Environ Microbiol 76:4538–4541
Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Sinninghe Damste JS, Kim GJ, Madsen EL, Rhee SK (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
Kim JG, Jung MY, Park SJ, Rijpstra WI, Sinninghe Damste JS, Madsen EL, Min D, Kim JS, Kim GJ, Rhee SK (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ Microbiol 14:1528–1543
Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546
Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci U S A 104:7104–7109
Laura E. Lehtovirta-Morley KS, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci U S A 108: 15892–15897
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
Liu S, Shen L, Lou L, Tian G, Zheng P, Hu B (2013) Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the Qiantang River, China. Appl Environ Microbiol 79:4065–4071
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
Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162–1175
Molina V, Belmar L, Ulloa O (2010) High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygen-deficient waters of the eastern South Pacific. Environ Microbiol 12:2450–2465
Park HD, Noguera DR (2007) Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations. J Appl Microbiol 102:1401–1417
Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76:7575–7587
Parsons RJ, Nelson CE, Carlson CA, Denman CC, Andersson AJ, Kledzik AL, Vergin KL, McNally SP, Treusch AH and Giovannoni SJ (2014) Marine bacterioplankton community turnover within seasonally hypoxic waters of a subtropical sound: Devil’s Hole, Bermuda. Environ Microbiol. doi:10.1111/1462-2920.12445
Peng X, Jayakumar A, Ward BB (2013) Community composition of ammonia-oxidizing archaea from surface and anoxic depths of oceanic oxygen minimum zones. Front Microbiol 4:177
Pester M, Rattei T, Flechl S, Grongroft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539
Pett-Ridge J, Petersen DG, Nuccio E, Firestone MK (2013) Influence of oxic/anoxic fluctuations on ammonia oxidizers and nitrification potential in a wet tropical soil. FEMS Microbiol Ecol 85:179–194
Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart GJ, Sinninghe Damste JS (2011) Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J 5:1896–1904
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
Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structure gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
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. Environ Microbiol 10:1601–1611
Shen LD, Liu S, Lou LP, Liu WP, Xu XY, Zheng P, Hu BL (2013) Broad distribution of diverse anaerobic ammonium-oxidizing bacteria in Chinese agricultural soils. Appl Environ Microbiol 79:6167–6172
Shen LD, Huang Q, He ZF, Lian X, Liu S, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2014) Vertical distribution of nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wetland soils. Appl Microbiol Biotechnol 99:349–357
Stewart FJ, Ulloa O, DeLong EF (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14:23–40
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
Yang Y, Shan J, Zhang J, Zhang X, Xie S, Liu Y (2014) Ammonia- and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils. Appl Microbiol Biotechnol 98:10197–10209
Zhang B, Fang F, Guo J, Chen Y, Li Z, Guo S (2012) Phosphorus fractions and phosphate sorption-release characteristics relevant to the soil composition of water-level-fluctuating zone of Three Gorges Reservoir. Ecol Eng 40:153–159
Acknowledgments
The authors wish to thank the National Science Foundation for Young Scientists of China (No. 51108408), the Fundamental Research Funds for the Central Universities (No. 2015QNA6012), and the Foundation from State Environmental Protection Key Laboratory of Microorganism Application and Risk Control of Tsinghua University (No. SMARC2013D004).
Conflict of interest
The authors declare that they have no competing interests.
Compliance with ethical standards
This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
ESM 1.
(PDF 216 kb)
Rights and permissions
About this article
Cite this article
Liu, S., Hu, B., He, Z. et al. Ammonia-oxidizing archaea have better adaptability in oxygenated/hypoxic alternant conditions compared to ammonia-oxidizing bacteria. Appl Microbiol Biotechnol 99, 8587–8596 (2015). https://doi.org/10.1007/s00253-015-6750-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6750-7


