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Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

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  • 1.

    Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, et al. Global consequences of land use. Science. 2005;309:570–4.

    CAS  PubMed  Google Scholar 

  • 2.

    Rockström J, Steffen W, Noone K, Persson Å, Chapin FS, Lambin EF, et al. A safe operating space for humanity. Nature. 2009;461:472–5.

    Google Scholar 

  • 3.

    Graham EB, Knelman JE, Schindlbacher A, Siciliano S, Breulmann M, Yannarell A, et al. Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol. 2016;7:1–10.

    Google Scholar 

  • 4.

    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 5.

    Hoegh-Guldberg O, Jacob D, Taylor M, Bindi M, Brown S, Camilloni I, et al. Impacts of 1.5 °C global warming on natural and human systems. In: Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, et al., editors. Geneva, Switzerland: World Meteorological Organization Technical Document; 2018.

  • 6.

    Dieleman WIJ, Vicca S, Tingey D, De Angelis P, Hagedorn F, Morgan JA, et al. Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO 2 and temperature. Glob Chang Biol. 2012;18:2681–93.

    PubMed  Google Scholar 

  • 7.

    Song J, Wan S, Piao S, Knapp AK, Classen AT, Vicca S, et al. A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat Ecol Evol. 2019;3:1309–20.

    PubMed  Google Scholar 

  • 8.

    Kuypers MMM, Marchant HK, Kartal B. The microbial nitrogen-cycling network. Nat Rev Microbiol. 2018;16:263–76. Nature Publishing Group.

    CAS  PubMed  Google Scholar 

  • 9.

    Prosser JI, Nicol GW. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 2012;20:523–31.

  • 10.

    Martens-Habbena W, Berube PM, Urakawa H, De La Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature. 2009;461:976–9.

    CAS  PubMed  Google Scholar 

  • 11.

    Fuchslueger L, Kastl EM, Bauer F, Kienzl S, Hasibeder R, Ladreiter-Knauss T, et al. Effects of drought on nitrogen turnover and abundances of ammonia-oxidizers in mountain grassland. Biogeosciences. 2014;11:6003–15.

    Google Scholar 

  • 12.

    Kits KD, Pjevac P, Daebeler A, Han P, Albertsen M, Romano S, et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature. 2017;549:269–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 13.

    Di HJ, Cameron KC, Shen JP, Winefield CS, Ocallaghan M, Bowatte S, et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci. 2009;2:621–4.

    CAS  Google Scholar 

  • 14.

    Jia Z, Conrad R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol. 2009;11:1658–71.

    CAS  PubMed  Google Scholar 

  • 15.

    Zhalnina K, Dörr de Quadros P, Camargo FAO, Triplett EW. Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol. 2012;3:1–9.

    Google Scholar 

  • 16.

    Gruber-Dorninger C, Pester M, Kitzinger K, Savio DF, Loy A, Rattei T, et al. Functionally relevant diversity of closely related Nitrospira in activated sludge. ISME J. 2015;9:643–55.

    CAS  PubMed  Google Scholar 

  • 17.

    Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, et al. Complete nitrification by Nitrospira bacteria. Nature. 2015;528:504–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 18.

    van Kessel MAHJ, Kartal B, MSM Jetten, Albertsen M, Op den Camp HJM, Lücker S, et al. Complete nitrification by a single microorganism. Nature. 2015;528:555–9.

    PubMed  PubMed Central  Google Scholar 

  • 19.

    Poghosyan L, Koch H, Lavy A, Frank J, van Kessel MAHJ, Jetten MSM, et al. Metagenomic recovery of two distinct comammox Nitrospira from the terrestrial subsurface. Environ Microbiol. 2019;00:1–11.

    Google Scholar 

  • 20.

    Wang Z, Cao Y, Zhu-Barker X, Nicol GW, Wright AL, Jia Z, et al. Comammox Nitrospira clade B contributes to nitrification in soil. Soil Biol Biochem. 2019;135:392–5.

    CAS  Google Scholar 

  • 21.

    Dusenge ME, Duarte AG, Way DA. Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. N. Phytol. 2019;221:32–49. John Wiley & Sons, Ltd.

    CAS  Google Scholar 

  • 22.

    de Graaff MA, van Groenigen KJ, Six J, Hungate B, van Kessel C. Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Chang Biol. 2006;12:2077–91.

    Google Scholar 

  • 23.

    Kuzyakov Y, Horwath WR, Dorodnikov M, Blagodatskaya E. Review and synthesis of the effects of elevated atmospheric CO2 on soil processes: No changes in pools, but increased fluxes and accelerated cycles. Soil Biol Biochem. 2019;128:66–78.

    CAS  Google Scholar 

  • 24.

    Luo Y, Su B, Currie WS, Dukes J. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience. 2004;54:731–9.

  • 25.

    Liang J, Qi X, Souza L, Luo Y. Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis. Biogeosciences. 2016;13:2689–99.

    CAS  Google Scholar 

  • 26.

    He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, et al. Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett. 2010;13:564–75.

    PubMed  Google Scholar 

  • 27.

    Horz HP, Barbrook A, Field CB, Bohannan BJM. Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci USA. 2004;101:15136–41.

    CAS  PubMed  Google Scholar 

  • 28.

    Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett. 2008;11:1316–27.

    PubMed  Google Scholar 

  • 29.

    Liu Q, Piao S, Janssens IA, Fu Y, Peng S, Lian X, et al. Extension of the growing season increases vegetation exposure to frost. Nat Commun. 2018;9:426.

    PubMed  PubMed Central  Google Scholar 

  • 30.

    Lax S, Abreu CI, Gore J. Higher temperatures generically favour slower-growing bacterial species in multispecies communities. Nat Ecol Evol. 2020;4:560–657.

    PubMed  Google Scholar 

  • 31.

    Tourna M, Freitag TE, Nicol GW, Prosser JI. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol. 2008;10:1357–64.

    CAS  PubMed  Google Scholar 

  • 32.

    Fierer N, Carney KM, Horner-Devine MC, Megonigal JP. The biogeography of ammonia-oxidizing bacterial communities in soil. Micro Ecol. 2009;58:435–45.

    Google Scholar 

  • 33.

    Schimel JP. Life in dry soils: effects of drought on soil microbial communities and processes. Annu Rev Ecol Evol Syst. 2018;49:409–32.

    Google Scholar 

  • 34.

    Kuzyakov Y, Horwath WR, Dorodnikov M, Blagodatskaya E. Review and synthesis of the effects of elevated atmospheric CO2 on soil processes: No changes in pools, but increased fluxes and accelerated cycles. Soil Biol Biochem. 2019;128:66–78.

  • 35.

    Yue K, Peng Y, Fornara DA, Van Meerbeek K, Vesterdal L, Yang W, et al. Responses of nitrogen concentrations and pools to multiple environmental change drivers: a meta-analysis across terrestrial ecosystems. Glob Ecol Biogeogr. 2019;28:690–724.

    Google Scholar 

  • 36.

    Bai E, Li S, Xu W, Li W, Dai W, Jiang P. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. N. Phytol. 2013;199:431–40.

    CAS  Google Scholar 

  • 37.

    Piepho HP, Herndl M, Pötsch EM, Bahn M. Designing an experiment with quantitative treatment factors to study the effects of climate change. J Agron Crop Sci. 2017;203:584–92.

    CAS  Google Scholar 

  • 38.

    Vance ED, Brookes PC, Jenkinson DS. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem. 1987;19:703–7.

    CAS  Google Scholar 

  • 39.

    Hood-Nowotny R, Umana NH-N, Inselbacher E, Oswald- Lachouani P, Wanek W. Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci Soc Am J. 2010;74:1018–27.

    CAS  Google Scholar 

  • 40.

    Wanek W, Mooshammer M, Blöchl A, Hanreich A, Richter A. Determination of gross rates of amino acid production and immobilization in decomposing leaf litter by a novel 15N isotope pool dilution technique. Soil Biol Biochem. 2010;42:1293–302.

    CAS  Google Scholar 

  • 41.

    Sørensen P, Jensen ES. Sequential diffusion of ammonium and nitrate from soil extracts to a polytetrafluoroethylene trap for 15N determination. Anal Chim Acta. 1991;252:201–3.

    Google Scholar 

  • 42.

    Lachouani P, Frank AH, Wanek W. A suite of sensitive chemical methods to determine the δ 15N of ammonium, nitrate and total dissolved N in soil extracts. Rapid Commun Mass Spectrom. 2010;24:3615–23.

    CAS  PubMed  Google Scholar 

  • 43.

    Angel R, Claus P, Conrad R. Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 2012;6:847–62.

    CAS  PubMed  Google Scholar 

  • 44.

    Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Micro Ecol. 2015;75:129–37.

    Google Scholar 

  • 45.

    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.

    CAS  PubMed  Google Scholar 

  • 46.

    Herbold CW, Pelikan C, Kuzyk O, Hausmann B, Angel R, Berry D, et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front Microbiol. 2015;6:1–8.

    Google Scholar 

  • 47.

    Purkhold U, Wagner M, Timmermann G, Pommerening-Röser A, Koops HP. 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol. 2003;53:1485–94.

    CAS  PubMed  Google Scholar 

  • 48.

    Alves RJE, Minh BQ, Urich T, Von Haeseler A, Schleper C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun. 2018;9:1–17.

    CAS  Google Scholar 

  • 49.

    Berger SA, Krompass D, Stamatakis A. Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol. 2011;60:291–302.

    PubMed  PubMed Central  Google Scholar 

  • 50.

    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 51.

    Aigle A, Prosser JI, Gubry-Rangin C. The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers. Environ Microbiome. 2019;14:3.

    Google Scholar 

  • 52.

    Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MAHJ, Daebeler A, et al. AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Microbiol. 2017;8:1–11.

    Google Scholar 

  • 53.

    Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 54.

    Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:W232–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 55.

    Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 56.

    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 57.

    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 58.

    Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol. 2014;16:3055–71.

    CAS  PubMed  Google Scholar 

  • 59.

    Sauder LA, Albertsen M, Engel K, Schwarz J, Nielsen PH, Wagner M, et al. Correction: cultivation and characterization of Candidatus nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J. 2020.

  • 60.

    Kozak M, Piepho HP. What’s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions. J Agron Crop Sci. 2018;204:86–98.

    Google Scholar 

  • 61.

    Langsrud Ø. ANOVA for unbalanced data: use type II instead of Type III sums of squares. Stat Comput. 2003;13:163–7.

    Google Scholar 

  • 62.

    McMurdie PJ, Holmes S. phyloseq: an R Package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 63.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan.

  • 64.

    Stier AC, Geange SW, Hanson KM, Bolker BM. Predator density and timing of arrival affect reef fish community assembly. Ecology. 2013;94:1057–68.

    PubMed  Google Scholar 

  • 65.

    Anderson MJ. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. Chichester, UK: John Wiley & Sons, Ltd; 2017. p 1–15.

  • 66.

    Fierer N, Schimel JP. A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J. 2010;67:798.

    Google Scholar 

  • 67.

    Lehtovirta-Morley LE. Ammonia oxidation: ecology, physiology, biochemistry and why they must all come together. FEMS Microbiol Lett. 2018;365:1–9.

    Google Scholar 

  • 68.

    Schimel JP, Schaeffer SM. Microbial control over carbon cycling in soil. Front Microbiol. 2012;3:1–11.

    Google Scholar 

  • 69.

    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.

    CAS  PubMed  Google Scholar 

  • 70.

    Larsen KS, Andresen LC, Beier C, Jonasson S, Albert KR, Ambus P, et al. Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Glob Chang Biol. 2011;17:1884–99.

    Google Scholar 

  • 71.

    Brenzinger K, Kujala K, Horn MA, Moser G, Guillet C, Kammann C, et al. Soil conditions rather than long-term exposure to elevated CO2 affect soil microbial communities associated with N-cycling. Front Microbiol. 2017;8:1–14.

    Google Scholar 

  • 72.

    Rütting T, Hovenden MJ. Soil nitrogen cycle unresponsive to decadal long climate change in a Tasmanian grassland. Biogeochemistry. 2020;147:99–107.

    Google Scholar 

  • 73.

    Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia. 2001;126:543–62.

    CAS  PubMed  Google Scholar 

  • 74.

    Fuchslueger L, Wild B, Mooshammer M, Takriti M, Kienzl S, Knoltsch A, et al. Microbial carbon and nitrogen cycling responses to drought and temperature in differently managed mountain grasslands. Soil Biol Biochem. 2019;135:144–53.

    CAS  Google Scholar 

  • 75.

    Coskun D, Britto DT, Shi W, Kronzucker HJ. Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nat Plants. 2017;3:17074.

    CAS  PubMed  Google Scholar 

  • 76.

    Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, et al. Suppression of soil nitrification by plants. Plant Sci. 2015;233:155–64.

    CAS  PubMed  Google Scholar 

  • 77.

    Canarini A, Dijkstra FA. Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol Biochem. 2015;81:195–203.

    CAS  Google Scholar 

  • 78.

    Karlowsky S, Augusti A, Ingrisch J, Akanda MKU, Bahn M, Gleixner G. Drought-induced accumulation of root exudates supports post-drought recovery of microbes in mountain grassland. Front Plant Sci. 2018;871:1–16.

    Google Scholar 

  • 79.

    Manzoni S, Schimel JP, Barbara S. Results from a responses of soil microbial communities to water stress: results from a meta-analysis. Ecology. 2017;93:930–8.

    Google Scholar 

  • 80.

    Canarini A, Merchant A, Dijkstra FA. Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere. 2016;2:85–97.

    Google Scholar 

  • 81.

    Hashem A, Kumar A, Al-Dbass AM, Alqarawi AA, Al-Arjani A-BF, Singh G, et al. Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi J Biol Sci. 2019;26:614–24.

    CAS  PubMed  Google Scholar 

  • 82.

    Williams A, de Vries FT. Plant root exudation under drought: implications for ecosystem functioning. N. Phytol. 2020;225:1899–1905.

    Google Scholar 

  • 83.

    Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, et al. Biological nitrification inhibition (BNI)—Is it a widespread phenomenon? Plant Soil. 2007;294:5–18.

    CAS  Google Scholar 

  • 84.

    Homyak PM, Allison SD, Huxman TE, Goulden ML, Treseder KK. Effects of drought manipulation on soil nitrogen cycling: a meta-analysis. J Geophys Res Biogeosci. 2017;122:3260–72.

    CAS  Google Scholar 

  • 85.

    Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. N. Phytol. 2014;201:916–27.

    CAS  Google Scholar 

  • 86.

    Thion C, Prosser JI. Differential response of nonadapted ammonia-oxidising archaea and bacteria to drying-rewetting stress. FEMS Microbiol Ecol. 2014;90:380–9.

    CAS  PubMed  Google Scholar 

  • 87.

    Norton JM, Klotz MG, Stein LY, Arp DJ, Bottomley PJ, Chain PSG, et al. Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol. 2008;74:3559–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 88.

    Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, et al. The genome of the ammonia-oxidizing CandidatusNitrososphaera gargensis: Insights into metabolic versatility and environmental adaptations. Environ Microbiol. 2012;14:3122–45.

    CAS  PubMed  Google Scholar 

  • 89.

    Kerou M, Offre P, Valledor L, Abby SS, Melcher M, Nagler M, et al. Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. Proc Natl Acad Sci USA. 2016;113:E7937–46.

    CAS  PubMed  Google Scholar 

  • 90.

    Nicol GW, Hink L, Gubry-Rangin C, Prosser JI, Lehtovirta-Morley LE. Genome Sequence of “ Candidatus Nitrosocosmicus franklandus” C13, a terrestrial ammonia-oxidizing archaeon. Microbiol Resour Announc. 2019;8:1–3.

    Google Scholar 

  • 91.

    Sauder LA, Albertsen M, Engel K, Schwarz J, Nielsen PH, Wagner M, et al. Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J. 2017;11:1142–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 92.

    Lehtovirta-Morley LE, Ge C, Ross J, Yao H, Nicol GW, Prosser JI. Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. FEMS Microbiol Ecol. 2014;89:542–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 93.

    Stieglmeier M, Klingl A, Alves RJE, Rittmann SKMR, Melcher M, Leisch N, et al. Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. Int J Syst Evol Microbiol. 2014;64:2738–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 94.

    Jung MY, Kim JG, Sinninghe Damsté JS, Rijpstra WIC, Madsen EL, Kim SJ, et al. A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment. Environ Microbiol Rep. 2016;8:983–92.

    CAS  PubMed  Google Scholar 

  • 95.

    Gwak JH, Jung MY, Hong H, Kim JG, Quan ZX, Reinfelder JR, et al. Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants. ISME J. 2020;14:335–46.

    CAS  PubMed  Google Scholar 

  • 96.

    Nowka B, Daims H, Spieck E. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl Environ Microbiol. 2015;81:745–53.

    PubMed  PubMed Central  Google Scholar 

  • 97.

    Prosser JI. The ecology of nitrifying bacteria. In: Bothe H, Ferguson SJ, editors. Newton WEBT-B of the NC. Biology of the Nitrogen Cycle. Amsterdam: Elsevier; 2007. p 223–43.

  • 98.

    Norton JM, Stark JM. Regulation and measurement of nitrification in terrestrial systems. In: Klotz MGBT-M in E. Research on nitrification and related processes, Part A. 2011. Academic Press, United States, p 343–68.

  • 99.

    Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Lücker S, et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science. 2014;345:1052 LP–1054.

    Google Scholar 

  • 100.

    Koch H, Lücker S, Albertsen M, Kitzinger K, Herbold C, Spieck E, et al. Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc Natl Acad Sci USA. 2015;112:11371–6.

    CAS  PubMed  Google Scholar 

  • 101.

    Daebeler A, Bodelier PLE, Yan Z, Hefting MM, Jia Z, Laanbroek HJ. Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil. ISME J. 2014;8:2397–410.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 102.

    Kim DG, Vargas R, Bond-Lamberty B, Turetsky MR. Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research. Biogeosciences. 2012;9:2459–83.

    CAS  Google Scholar 

  • 103.

    Wrage N, Velthof GL, Van Beusichem ML, Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem. 2001;33:1723–32.

    CAS  Google Scholar 

  • 104.

    Stein LY. Surveying N2O-producing pathways in bacteria. In: Klotz MGBT-M in E. Research on nitrification and related processes, Part A. 2011. Academic Press, United States, pp 131–52.

  • 105.

    Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J. 2016;10:1836–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 106.

    Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, et al. Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata. Nat Commun. 2019;10:1–12.

    CAS  Google Scholar 


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