Environmental Factors Leading to the Niche Segregation of Ammonia-Oxidizing Archaea and Ammonia-Oxidizing Bacteria in Nature

VIEWS - 54 (Abstract) 16 (PDF)
Shuai Liu, Jiajie Hu, Jiaxian Shen, Shu Chen, Guangming Tian, Ping Zheng, Liping Lou, Fang Ma, Baolan Hu


Ammonia oxidation is an important step of the nitrogen cycle and was considered to be conducted only by bacteria for a long time. The discovery of ammonia-oxidizing archaea (AOA) caused consideration of the relative contributions of these two functional groups in different niches and factors resulting in their niche segregation. Previous studies showed that many environmental factors may correlate to the abundance and distribution of AOA and AOB, including ammonia/ammonium concentration, pH, organic matters, oxygen concentration, temperature, salinity, sulfide concentration, phosphate concentration, soil moisture, and others. To understand the effects of environmental factors on AOA and AOB, five main environmental factors which may be related to each other were selectively reviewed independently. Here, we discuss the influences of ammonia concentration, pH, temperature, oxygen concentration and organic matters on the niche segregation of AOA and AOB, and try to explain ecology phenomena from physiological and genic level.


ammonia concentration; pH; temperature; oxygen concentration; organic matters

Full Text:



Monteiro M, Seneca J and Magalhaes C, 2014, The history of aerobic ammonia oxidizers: from the first discoveries to today. Journal of Microbiology. 52:537-47. http://dx.doi.org/10.1007/s12275-014-4114-0

Lehtovirta-Morley L E, Stoecker K, Vilcinskas A, et al. 2011, Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proceedings of The National Academy of Sciences of The United States of America. 108:15892-15897. http://dx.doi.org/10.1073/pnas.1107196108

Jung M Y, Park S J, Min D, 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. http://dx.doi.org/10.1128/AEM.05787-11

Kim J G, Jung M Y, Park S J, et al. 2012, Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environmental Microbiology. 14:1528-1543. http://dx.doi.org/10.1111/j.1462-2920.2012.02740.x

Jung M Y, Park S J, Kim S J, et al. 2014, A Mesophilic, Autotrophic, Ammonia-Oxidizing Archaeon of Thaumarchaeal Group I.1a Cultivated from a Deep Oligotrophic Soil Horizon. Applied And Environmental Microbiology. 80:3645-3655. http://dx.doi.org/10.1128/AEM.03730-13

Hatzenpichler R, Lebedeva E V, Spieck E, et al. 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. http://dx.doi.org/10.1073/pnas.0708857105

de la Torre J R, Walker C B, Ingalls A E, et al. 2008, Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environmental Microbiology. 10:810 - 818. http://dx.doi.org/10.1111/j.1462-2920.2007.01506.x

Blainey P C, Mosier A C, Potanina A, et al. 2011, Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626. http://dx.doi.org/10.1371/journal.pone.0016626

Mosier A C, Allen E E, Kim M, et al. 2012, Genome sequence of "Candidatus Nitrosopumilus salaria" BD31, an ammonia-oxidizing archaeon from the San Francisco Bay estuary. Journal of Bacteriology. 194:2121-2. http://dx.doi.org/10.1128/JB.00013-12

DeLong E, Hallam S, Mincer T, et al. 2006, Correction: Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. Plos Biology. 4: 2412-2412. http://dx.doi.org/10.1371/journal.pbio.0040437

Biller S J, Mosier A C, Wells G F, et al. 2012, Global Biodiversity of Aquatic Ammonia-Oxidizing Archaea is Partitioned by Habitat. Frontiers In Microbiology. 3:252. http://dx.doi.org/10.3389/fmicb.2012.00252

Wuchter C, Abbas B, Coolen M J L, et al. 2006, Archaeal nitrification in the ocean. Proceedings of The National Academy of Sciences of The United States of America. 103:12317-22. http://dx.doi.org/10.1073/pnas.0600756103

Leininger S, Urich T, Schloter M, et al. 2006, Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. http://dx.doi.org/10.1038/nature04983

Verhamme D T, Prosser J I and Nicol G W, 2011, Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. Isme Journal. 5:1067–1071. http://dx.doi.org/10.1038/ismej.2010.191

Gubry-Rangin C, Hai B, Quince C, et al. 2011, Niche specialization of terrestrial archaeal ammonia oxidizers. Proceedings of The National Academy of Sciences of The United States of America. 108:21206-21211. http://dx.doi.org/10.1073/pnas.1109000108

Qin W, Amin S A, Martens-Habbena W, et al. 2014, Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proceedings of The National Academy of Sciences of The United States of America. 111: 12504-12509. http://dx.doi.org/10.1073/pnas.1324115111

Santoro A E, Francis C A, de Sieyes N R, et al. 2008, Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology. 10:1068 –1079. http://dx.doi.org/10.1111/j.1462-2920.2007.01547.x

Hatzenpichler R, 2012, Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Applied And Environmental Microbiology. 78(21):7501-10. http://dx.doi.org/10.1128/AEM.01960-12

Stahl D A and de la Torre J R, 2012, Physiology and diversity of ammonia-oxidizing archaea. Annual Review of Microbiology. 66: 83-101. http://dx.doi.org/10.1146/annurev-micro-092611-150128

Martens-Habbena W, Berube P M, Urakawa H, et al. 2009, Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976 –979. http://dx.doi.org/10.1038/nature08465

Könneke M, Bernhard A E, de la Torre J R, et al. 2005, Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-546. http://dx.doi.org/10.1038/nature03911

Tourna M, Stieglmeier M, Spang A, 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. http://dx.doi.org/10.1073/pnas.1013488108

Lehtovirta-Morley L E, Ross J, Hink L, et al. 2016, Isolation of ‘Candidatus Nitrosocosmicus franklandus’, a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration. Fems Microbiology Ecology. 92(5):fiw057. doi: 10.1093/femsec/fiw057

Suwa Y, Imamura Y, Suzuki T, et al. 1994, Ammonia-oxidizing bacteria with different sensitivities to (NH4)2SO4 in activated sludges. Water Res. 28:1523-1532. http://dx.doi.org/10.1016/0043-1354(94)90218-6

Koops H P, Purkhold U, Pommerening-Röser A, et al. 2003, The lithoautotrophic ammonia-oxidizing bacteria. The Procaryotes: An Evolving Electronic Resource for the Microbiological Community, third edition ed. Springer-Verlag, New York. 5: 778-811.

Prosser J I and Nicol G W, 2012, Archaeal and bacterial ammonia oxidisers in soil: the quest for niche specialisation and differentiation. Trends In Microbiology. 20: 523-532. http://dx.doi.org/10.1016/j.tim.2012.08.001

Yang O, Norton J M, Stark J M, et al. 2016, Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biology & Biochemistry, 96:4-15. http://dx.doi.org/10.1016/j.soilbio.2016.01.012

Norman J S and Barrett J E, 2014, Substrate and nutrient limitation of ammonia-oxidizing bacteria and archaea in temperate forest soil. Soil Biology & Biochemistry, 69(1):141-146. http://dx.doi.org/10.1016/j.soilbio.2013.11.003

Zhang X, Tang Y, Shi Y, et al. 2016, Responses of soil hydrolytic enzymes, ammonia-oxidizing bacteria and archaea to nitrogen applications in a temperate grassland in Inner Mongolia. Scientific Reports, 6(6):32791. http://dx.doi.org/10.1038/srep32791

Lagostina L, Goldhammer T, Røy H, et al. 2015, Ammonia-oxidizing Bacteria of the N itrosospira cluster 1 dominate over ammonia-oxidizing Archaea in oligotrophic surface sediments near the South Atlantic Gyre. Environmental Microbiology Reports. 7:404-413. doi:10.1111/1758-2229.12264

Herrmann M, Scheibe A, Avrahami S, et al. 2011, Ammonium availability affects the ratio of ammonia-oxidizing bacteria to ammonia-oxidizing archaea in simulated creek ecosystems. Applied & Environmental Microbiology, 77(5):1896. http://dx.doi.org/10.1128/AEM.02879-10

Yang Y, Zhang J, Zhao Q, et al. 2016, Sediment Ammonia-Oxidizing Microorganisms in Two Plateau Freshwater Lakes at Different Trophic States. Microbial Ecology, 71(2):257. http://dx.doi.org/10.1007/s00248-015-0642-3

Sauder L A, Peterse F, Schouten S, et al. 2012, Low-ammonia niche of ammonia-oxidizing archaea in rotating biological contactors of a municipal wastewater treatment plant. Environmental Microbiology. 14: 2589-2600. http://dx.doi.org/10.1111/j.1462-2920.2012.02786.x

Burton S A Q and Prosser J I, 2001, Autotrophic ammonia oxidation at low pH through urea hydrolysis. Applied And Environmental Microbiology. 67:2952-2957. http://dx.doi.org/10.1128/AEM.67.7.2952-2957.2001

von Uexküll H R and Mutert E, 1995, Plant-Soil Interactions at Low pH, Principles and Management, eds Date RA, Grundon NJ, Raymet GE, Probert ME (Kluwer, New York), pp 5e19.

Lu L and Jia Z, 2012, Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environmental Microbiology. 15: 1-15. https://doi.org/10.1111/1462-2920.12071

Lehtovirta-Morley L E, Sayavedra-Soto L A, Gallois N, et al. 2016, Identifying potential mechanisms enabling acidophily in the ammonia-oxidising archaeon ‘Candidatus Nitrosotalea devanaterra’. Applied And Environmental Microbiology. 82(9):2608-19. http://dx.doi.org/10.1128/AEM.04031-15

Nicol G W, Leininger S, Schleper C, et al. 2008, The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology. 10: 2966-2978. http://dx.doi.org/10.1111/j.1462-2920.2008.01701.x

He J Z, Shen J P, Zhang L M, et al. 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. http://dx.doi.org/10.1111/j.1462-2920.2007.01481.x

Hu B L, Liu S, Wang W, et al. 2014, pH-dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. Fems Microbiology Ecology. 90: 290-299. http://dx.doi.org/10.1111/1574-6941.12391

Stempfhuber B, Engel M, Fischer D, et al. 2015, pH as a Driver for Ammonia-Oxidizing Archaea in Forest Soils. Microbial Ecology. 69:879-883. http://dx.doi.org/10.1007/s00248-014-0548-5

Norman J S and Barrett J E, 2016, Substrate availability drives spatial patterns in richness of ammonia-oxidizing bacteria and archaea in temperate forest soils. Soil Biology & Biochemistry, 94:169-172. http://dx.doi.org/10.1016/j.soilbio.2015.11.015

Gan X H, Zhang F Q, Gu J D, et al. 2016, Differential distribution patterns of ammonia-oxidizing archaea and bacteria in acidic soils of Nanling National Nature Reserve forests in subtropical China. Antonie Van Leeuwenhoek, 109(2):237-251. http://dx.doi.org/10.1007/s10482-015-0627-8

Stopnisek N, Gubry-Rangin C, Hofferle S, et al. 2010, Thaumarchaeal Ammonia Oxidation in an Acidic Forest Peat Soil Is Not Influenced by Ammonium Amendment. Applied And Environmental Microbiology. 76: 7626-7634. http://dx.doi.org/10.1128/AEM.00595-10

Yao H, Gao Y, Nicol G W, et al. 2011, Links between Ammonia Oxidizer Community Structure, Abundance, and Nitrification Potential in Acidic Soils. Applied And Environmental Microbiology. 77: 4618-4625. http://dx.doi.org/10.1128/AEM.00136-11

Zhou Z F, Wang M X, Liu W L, et al. 2015, A comparative study of ammonia-oxidizing archaea and bacteria in acidic and alkaline purple soils. Annals of Microbiology.66(2):615. http://dx.doi.org/10.1007/s13213-015-1143-9

Song H, Che Z, Cao W C, et al. 2016, Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen. Environmental Science & Pollution Research International, 23(12):11964-11974. http://dx.doi.org/10.1007/s11356-016-6396-8

Taylor A E, Giguere A T, Zoebelein C M, et al. 2016, Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. Isme Journal. 11(4):896. http://dx.doi.org/10.1038/ismej.2016.179

Reigstad L J, Richter A, Daims H, et al. 2008, Nitrification in terrestrial hot springs of Iceland and Kamchatka. Fems Microbiology Ecology. 64:167–174. http://dx.doi.org/10.1111/j.1574-6941.2008.00466.x

Park B J, Park S J, Yoon D N, et al. 2010, Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Applied And Environmental Microbiology. 76: 7575-7587. http://dx.doi.org/10.1128/AEM.01478-10

Dalsgaard T, Stewart F, De Brabandere L, et al. 2013, The effects of oxygen on process rates and gene expression of anammox and denitrification in the Eastern South Pacific oxygen minimum zone. Abstract retrieved from ASLO 2013 Aquatic Sciences Meeting. (Accession No. 2282377314)

Park H D and Noguera D R, 2007, Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations. Journal of Applied Microbiology. 102: 1401-1417. http://dx.doi.org/10.1111/j.1365-2672.2006.03176.x

Kim J G, Park S J, Sinninghe Damsté J S, et al. 2016, Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proceedings of The National Academy of Sciences of The United States of America.113(28). http://dx.doi.org/10.1073/pnas.1605501113

Abell G C, Banks J, Ross D J, et al. 2011, Effects of estuarine sediment hypoxia on nitrogen fluxes and ammonia oxidizer gene transcription. Fems Microbiology Ecology. 75: 111-122. http://dx.doi.org/10.1111/j.1574-6941.2010.00988.x

Ke X, Lu W and Conrad R, 2015, High Oxygen Concentration Increases the Abundance and Activity of Bacterial Rather than Archaeal Nitrifiers in Rice Field Soil. Microbial Ecology, 70(4):961. http://dx.doi.org/10.1007/s00248-015-0633-4

Lu S M, Liu X G, Ma Z J, et al. 2016, Vertical Segregation and Phylogenetic Characterization of Ammonia-Oxidizing Bacteria and Archaea in the Sediment of a Freshwater Aquaculture Pond. Frontiers In Microbiology. 6:177-183. http://dx.doi.org/10.3389/fmicb.2015.01539

Molina V, Belmar L and Ulloa O, 2010, High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygen-deficient waters of the eastern South Pacific. Environmental Microbiology. 12: 2450-2465. http://dx.doi.org/10.1111/j.1462-2920.2010.02218.x

Vissers E W, Anselmetti F S, Bodelier P L, et al. 2013, Temporal and spatial coexistence of archaeal and bacterial amoA genes and gene transcripts in Lake Lucerne. Archaea. 1-13. doi: 10.1155/2013/289478

Liu S, Hu B L, He Z F, et al. 2015, Ammonia-oxidizing archaea have better adaptability in oxygenated/hypoxic alternant conditions compared to ammonia-oxidizing bacteria. Applied Microbiology And Biotechnology. 99: 8587-8596. http://dx.doi.org/10.1007/s00253-015-6750-7

Lehtovirta-Morley L E, Ge C, Ross J, et al. 2014, Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. Fems Microbiology Ecology. 89:542-52. http://dx.doi.org/10.1111/1574-6941.12353

Jung M Y, Kim J G, Damsté J S S, et al. 2016, A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment. Environmental Microbiology Reports, 8(6). doi: 10.1111/1758-2229.12477

Bayer B, Vojvoda J, Offre P, et al. 2016, Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. Isme Journal, 10(5):1051. http://dx.doi.org/10.1038/ismej.2015.200

Kim J G, Park S J, Sinninghe Damsté J S, et al. 2016, Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proceedings of The National Academy of Sciences of The United States of America.113(28). http://dx.doi.org/10.1073/pnas.1605501113

Sauder L A, Albertsen M, Engel K, et al. 2017, Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. Isme Journal, 11(5):1142-1157. http://dx.doi.org/10.1038/ismej.2016.192

Ouverney C C and Fuhrman J A, 2000, Marine Planktonic Archaea Take Up Amino Acids. Appl Microbiol Biot. 66: 4829-4833. http://dx.doi.org/10.1128/AEM.66.11.4829-4833.2000

Agogué H, Brink M, Dinasquet J, et al. 2008, Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456:788 -791. http://dx.doi.org/10.1038/nature07735

Martin-Cuadrado A B, Rodriguez-Valera F, Moreira D, et al. 2008, Hindsight in the relative abundance, metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions. Isme Journal. 2: 865-886. http://dx.doi.org/10.1038/ismej.2008.40

Berg I A, Kockelkorn D, Ramos-Vera W H, et al. 2010, Autotrophic carbon fixation in archaea. Nature Reviews Microbiology. 8: 447-460. http://dx.doi.org/10.1038/nrmicro2365

Walker C B, de la Torre J R, Klotz M G, et al. 2010, Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of The National Academy of Sciences of The United States of America. 107:8818–8823. http://dx.doi.org/10.1073/pnas.0913533107

Gubry-Rangin C, Novotnik B, Mandič-Mulec I, et al. 2017, Temperature responses of soil ammonia-oxidising archaea depend on pH. Soil Biology & Biochemistry, 106:61-68. http://dx.doi.org/10.1016/j.soilbio.2016.12.007

van Kessel M A H J, Speth D R, Albertsen M, et al. 2015, Complete nitrification by a single microorganism. Nature, 528(7583):555. http://dx.doi.org/10.1038/nature16459

Daims H, Lebedeva E V, Pjevac P, et al. 2015, Complete nitrification by Nitrospira bacteria. Nature, 528(7583):504. http://dx.doi.org/10.1038/nature16461

DOI: http://dx.doi.org/10.26789/AEB.2017.01.004


  • There are currently no refbacks.

Copyright (c) 2017 Shuai Liu, Jiajie Hu, Jiaxian Shen, Shu Chen, Guangming Tian, Ping Zheng, Liping Lou, Fang Ma, Baolan Hu

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.