Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities

Abstract

Nitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co-occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major cultivated phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest affinity for both ammonia and total ammonium of any characterized AOA, and these values are similar to previously determined ammonia and total ammonium affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values supports the hypothesis that—like for AOB—ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.

References 92

1. 1.

   Ward BB, Arp DJ, Klotz MG. Nitrification. Washington, D.C.: American Society of Microbiology; 2011.

   Not in our library

2. 2.

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

   Not in our library10.1038/nrmicro.2018.9

3. 3.

   Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543-6.

   Not in our library10.1038/nature03911

4. 4.

   Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol. 2005;7:1985-95.

   Not in our library10.1111/j.1462-2920.2005.00906.x

5. 5.

   Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature. 2017;549:269-72.

   Not in our library10.1038/nature23679

6. 6.

   van Kessel MA, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJ, Kartal B, et al. Complete nitrification by a single microorganism. Nature. 2015;528:555-9.

   Not in our library10.1038/nature16459

7. 7.

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

   Not in our library10.1038/nature16461

8. 8.

   Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006;442:806-9.

   Not in our library10.1038/nature04983

9. 9.

   Verhamme DT, Prosser JI, Nicol GW. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011;5:1067-71.

   Not in our library10.1038/ismej.2010.191

10. 10.

    Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P, et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA. 2006;103:12317-22.

    Not in our library10.1073/pnas.0600756103

11. 11.

    Yang Y, Zhang J, Zhao Q, Zhou Q, Li N, Wang Y, et al. Sediment ammonia-oxidizing microorganisms in two plateau freshwater lakes at different trophic states. Microb Ecol. 2016;71:257-65.

    Not in our library10.1007/s00248-015-0642-3

12. 12.

    Fan F, Yang Q, Li Z, Wei D, Cui X, Liang Y. Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb Ecol. 2011;62:982-90.

    Not in our library10.1007/s00248-011-9897-5

13. 13.

    Bollmann A, Bullerjahn GS, McKay RM. Abundance and diversity of ammonia-oxidizing archaea and bacteria in sediments of trophic end members of the Laurentian Great Lakes, Erie and Superior. PLoS ONE. 2014;9:e97068.

    Not in our library10.1371/journal.pone.0097068

14. 14.

    Mußmann M, Brito I, Pitcher A, Sinninghe Damsté JS, Hatzenpichler R, Richter A, et al. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci USA. 2011;108:16771-6.

    Not in our library10.1073/pnas.1106427108

15. 15.

    Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, et al. Comammox in drinking water systems. Water Res. 2017;116:332-41.

    Not in our library10.1016/j.watres.2017.03.042

16. 16.
    AmoA-Targeted Polymerase Chain Reaction Primers for the Specific Detection and Quantification of Comammox Nitrospira in the Environment · 2017

    No notice
17. 17.

    Fowler SJ, Palomo A, Dechesne A, Mines PD, Smets BF. Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environ Microbiol. 2018;20:1002-15.

    Not in our library10.1111/1462-2920.14033

18. 18.

    Roots P, Wang Y, Rosenthal AF, Griffin JS, Sabba F, Petrovich M, et al. Comammox Nitrospira are the dominant ammonia oxidizers in a mainstream low dissolved oxygen nitrification reactor. Water Res. 2019;157:396-405.

    Not in our library10.1016/j.watres.2019.03.060

19. 19.

    Xia F, Wang JG, Zhu T, Zou B, Rhee SK, Quan ZX. Ubiquity and diversity of complete ammonia oxidizers (Comammox). Appl Environ Microbiol. 2018;84:e01390–18.

    Not in our library10.1128/aem.01390-18

20. 20.

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

    Not in our library10.1016/j.tim.2012.08.001

21. 21.

    Schleper C. Ammonia oxidation: different niches for bacteria and archaea? ISME J. 2010;4:1092-4.

    Not in our library10.1038/ismej.2010.111

22. 22.

    French E, Kozlowski JA, Mukherjee M, Bullerjahn G, Bollmann A. Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl Environ Microbiol. 2012;78:5773-80.

    Not in our library10.1128/aem.00432-12

23. 23.

    Merbt SN, Stahl DA, Casamayor EO, Marti E, Nicol GW, Prosser JI. Differential photoinhibition of bacterial and archaeal ammonia oxidation. FEMS Microbiol Lett. 2012;327:41-6.

    Not in our library10.1111/j.1574-6968.2011.02457.x

24. 24.

    Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Sinninghe Damsté JS, et al. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl Environ Microbiol. 2011;77:8635-47.

    Not in our library10.1128/aem.05787-11

25. 25.
    Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds · 2014

    No notice
26. 26.

    Sedlacek CJ, Giguere AT, Dobie MD, Mellbye BL, Ferrell RV, Woebken D et al. Transcriptomic response of Nitrosomonas europaea transitioned from ammonia- to oxygen-limited steady-state growth. mSystems. 2020;5:e00562–19.

    Not in our library10.1128/msystems.00562-19

27. 27.

    Gwak J-H, Jung M-Y, Hong H, Kim J-G, Quan Z-X, 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.

    Not in our library10.1038/s41396-019-0538-1

28. 28.

    Button DK. Biochemical basis for whole-cell uptake kinetics: specific affinity, oligotrophic capacity, and the meaning of the michaelis constant. Appl Environ Microbiol. 1991;57:2033-8.

    Not in our library10.1128/aem.57.7.2033-2038.1991

29. 29.

    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.

    Not in our library10.1038/nature08465

30. 30.

    Hatzenpichler R. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol. 2012;78:7501-10.

    Not in our library10.1128/aem.01960-12

31. 31.

    Aigle A, Gubry-Rangin C, Thion C, Estera-Molina KY, Richmond H, Pett-Ridge J, et al. Experimental testing of hypotheses for temperature- and pH-based niche specialization of ammonia oxidizing archaea and bacteria. Environ Microbiol. 2020;22:4032-45.

    Not in our library10.1111/1462-2920.15192

32. 32.

    Taylor AE, Giguere AT, Zoebelein CM, Myrold DD, Bottomley PJ. Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J. 2017;11:896-908.

    Not in our library10.1038/ismej.2016.179

33. 33.

    Groeneweg J, Sellner B, Tappe W. Ammonia oxidation in Nitrosomonas at NH3 concentrations near Km: effects of pH and temperature. Water Res. 1994;28:2561-6.

    Not in our library

34. 34.

    Jones RD, Morita RY. Low-temperature growth and whole-cell kinetics of a marine ammonium oxidizer. Mar Ecol Prog Ser. 1985;21:239-43.

    Not in our library

35. 35.

    Suzuki I, Dular U, Kwok SC. Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol. 1974;120:556-8.

    Not in our library10.1128/jb.120.1.556-558.1974

36. 36.

    Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils. 1988;6:68-72.

    Not in our library

37. 37.

    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.

    Not in our library

38. 38.

    Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 2001;5:62-71.

    Not in our library10.1006/niox.2000.0319

39. 39.
    Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata · 2019

    No notice
40. 40.

    Lebedeva EV, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S, Bulaev A, et al. Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS ONE. 2013;8:e80835.

    Not in our library10.1371/journal.pone.0080835

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.