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PreprintCited by 58Microbial metabolism and enzyme functionWastewater Treatment and Nitrogen RemovalMetal-Catalyzed Oxygenation Mechanisms

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Unexpected Complexity of the Ammonia Monooxygenase in Archaea

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Hodgskiss, Logan H., Melcher, Michael, Kerou, Melina, Chen, Weiqiang, Ponce-Toledo, Rafael I., Savvides, Savvas N., Wienkoop, Stefanie, Hartl, Markus, Schleper, Christa·2022·The ISME Journal
DOI 10.1101/2022.04.06.487334PMC PMC10030591

Preprint — published as 10.1038/s41396-023-01367-3

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Abstract

Ammonia oxidation as the first step of nitrification constitutes a critical process in the global nitrogen cycle. However, fundamental knowledge of its key enzyme, the copper-dependent ammonia monooxygenase is lacking, in particular for the environmentally abundant ammonia oxidizing archaea (AOA). Here, the structure of the enzyme is investigated by blue-native gel electrophoresis and proteomics from native membrane complexes of two AOA. Beside the known AmoABC subunits and the earlier predicted AmoX, two new protein subunits, AmoY and AmoZ, were identified. They are unique to AOA, highly conserved and co-regulated, and their genes are linked to other AMO subunit genes in streamlined AOA genomes. Modelling and in gel cross-link approaches support an overall protomer structure similar to the distantly related bacterial particulate methane monooxygenase indicating that AmoY and AmoZ serve an important structural and functional role. These data open avenues for further structure-function studies of this ecologically important key nitrification complex.

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Research works printed but not linked: 106

  1. 1975, The kinetics of microbial nitrification, Water Res, 9, 1099, 10.1016/0043-1354(75)90108-6 · DOI
  2. 10.1042/bj2270719 · DOI
  3. 1981, Oxidation of ammonia by Nitrosomonas europaea. Definite 18O-tracer evidence that hydroxylamine formation involves a monooxygenase, J. Biol. Chem, 256, 10834, 10.1016/S0021-9258(19)68518-2 · DOI
  4. 1890, Recherches sur les organismes de la nitrification, Ann Inst Pateur, 4, 213
  5. 10.1038/nature03911 · DOI
  6. 10.1111/j.1462-2920.2005.00906.x · DOI
  7. 10.1126/science.1093857 · DOI · Paper page
  8. 10.1038/nature04983 · DOI · Paper page
  9. 10.1111/j.1462-2920.2008.01701.x · DOI
  10. 10.1007/s00248-007-9360-9 · DOI
  11. 10.1038/35054051 · DOI
  12. 10.1038/ismej.2010.189 · DOI
  13. 10.1038/ismej.2012.64 · DOI
  14. 10.1038/ismej.2010.172 · DOI
  15. 10.1073/pnas.1601212113 · DOI
  16. Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. 107, (2010). · DOI
  17. Berg, I. A. , Kockelkorn, D. , Buckel, W. & Fuchs, G. A 3-Hydroxypropionate/4-Hydroxybutyrate Autotrophic Carbon Dioxide Assimilation Pathway in Archaea. Science (80-.). 318, (2007). · DOI
  18. 10.1073/pnas.1402028111 · DOI
  19. 10.1016/j.joule.2018.01.018 · DOI
  20. 2013, Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations, Biochim. Biophys. Acta -Bioenerg, 1827, 114, 10.1016/j.bbabio.2012.07.005 · DOI · Paper page
  21. 10.1038/ismej.2016.2 · DOI
  22. 10.1038/nature03311 · DOI
  23. 10.1042/BST0361134 · DOI
  24. 10.1021/bi200801z · DOI
  25. 10.1074/jbc.M114.581363 · DOI
  26. 10.1074/jbc.RA118.003348 · DOI
  27. 2021, Copper Centers in the Cryo-EM Structure of Particulate Methane Monooxygenase Reveal the Catalytic Machinery of Methane Oxidation, J. Am. Chem. Soc, 143, 9922, 10.1021/jacs.1c04082 · DOI
  28. 10.1038/nature08992 · DOI
  29. 10.1111/j.1758-2229.2009.00022.x · DOI
  30. 10.1126/science.aav2572 · DOI
  31. 2014, Mutagenesis of the hydrocarbon monooxygenase indicates a metal centre in subunit-C, and not subunit-B, is essential for copper-containing membrane monooxygenase activity, Microbiol. (United Kingdom), 160, 1267
  32. 2020, The model structure of the copper-dependent ammonia monooxygenase, JBIC J. Biol. Inorg. Chem, 1, 3
  33. 10.1038/s41467-018-03861-1 · DOI
  34. 10.3389/fmicb.2018.02493 · DOI
  35. 2012, Metagenomic Analysis of Ammonia-Oxidizing Archaea Affiliated with the Soil Group, Front. Microbiol, 0, 208
  36. 10.1038/nprot.2006.62 · DOI
  37. Abby, S. S. , Kerou, M. & Schleper, C. Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate. MBio 11, (2020). · DOI
  38. 2021, A standardized archaeal taxonomy for the Genome Taxonomy Database, Nat. Microbiol, 6, 946, 10.1038/s41564-021-00918-8 · DOI
  39. 10.3389/fmicb.2018.00803 · DOI
  40. 10.1016/j.tim.2006.03.004 · DOI
  41. Luo, Z.-H. et al. Genomic Insights of “Candidatus Nitrosocaldaceae” Based on Nine New Metagenome-Assembled Genomes, Including “Candidatus Nitrosothermus” Gen Nov. and Two New Species of “Candidatus Nitrosocaldus”. Front. Microbiol. 11, (2021). · DOI
  42. 10.15252/embj.2020106174 · DOI
  43. 10.1099/ijs.0.063172-0 · DOI
  44. 10.1038/nrmicro2576 · DOI · Paper page
  45. 2020, Genome wide transcriptomic analysis of the soil ammonia oxidizing archaeon Nitrososphaera viennensis upon exposure to copper limitation, ISME J, 14, 2659, 10.1038/s41396-020-0715-2 · DOI
  46. Qin, W. et al. Stress response of a marine ammonia-oxidizing archaeon informs physiological status of environmental populations. Nat. Publ. Gr. doi, (2017). · DOI
  47. 10.1111/1462-2920.14107 · DOI
  48. 10.1111/j.1462-2920.2010.02400.x · DOI
  49. Bayer, B. et al. Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium Downloaded from. msystems.asm.org vol. 4 http://msystems.asm.org/ (2019). · DOI
  50. 10.1073/pnas.1416223112 · DOI · Paper page
  51. 2017, Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea, Environ. Microbiol. Rep, 9, 484, 10.1111/1758-2229.12567 · DOI
  52. 10.1038/s41396-021-01177-5 · DOI
  53. 10.1016/j.jmb.2004.03.016 · DOI
  54. 10.1146/annurev.biochem.76.061505.175355 · DOI
  55. 2022, NAR Breakthrough Article AlphaFold Protein Structure Database : massively expanding the structural coverage of protein-sequence space with high-accuracy models, 50, 439
  56. 10.1007/978-1-61779-361-5_16 · DOI
  57. 10.1186/1471-2105-7-191 · DOI · Paper page
  58. 10.1111/j.1574-6968.2007.00970.x · DOI
  59. 10.1161/CIRCULATIONAHA.113.005224.Aldose · DOI
  60. 2019, Complexome analysis of the nitrite-dependent methanotroph Methylomirabilis lanthanidiphila, Biochim. Biophys. Acta -Bioenerg, 1860, 734, 10.1016/j.bbabio.2019.07.011 · DOI
  61. 10.1038/ismej.2009.138 · DOI
  62. 10.1038/nrmicro3260 · DOI
  63. 10.1194/jlr.M200148-JLR200 · DOI
  64. 10.1111/j.1462-2920.2007.01506.x · DOI
  65. 10.1128/AEM.01681-12 · DOI
  66. 10.1016/j.gca.2015.09.004 · DOI
  67. 10.1128/AEM.01654-07 · DOI
  68. 10.1038/s41467-018-02974-x · DOI · Paper page
  69. 10.1128/JB.01861-06 · DOI
  70. 10.1128/JB.00133-12 · DOI
  71. 10.1371/journal.pone.0054583 · DOI · Paper page
  72. 10.1099/ijsem.0.002416 · DOI
  73. 10.1038/s41396-018-0289-4 · DOI
  74. 10.1042/bj2120031 · DOI
  75. 10.1007/BF00414458 · DOI
  76. 10.1128/AEM.54.12.3187-3190.1988 · DOI
  77. 1983, Methane oxidation by Nitrosococcus oceanus and Nitrosomonas europaea, Appl. Environ. Microbiol, 45, 401, 10.1128/aem.45.2.401-410.1983 · DOI
  78. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, (2010). · DOI
  79. 10.1093/nar/gkf436 · DOI · Paper page
  80. 10.1093/molbev/mst010 · DOI · Paper page
  81. 10.1186/1471-2105-10-1 · DOI
  82. Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): A new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, (2010). · DOI
  83. 10.1093/molbev/msaa015 · DOI · Paper page
  84. 10.1093/molbev/msx281 · DOI · Paper page
  85. 10.1038/s41396-018-0091-3 · DOI
  86. 10.1038/nature12352 · DOI · Paper page
  87. 10.1073/pnas.1013488108 · DOI
  88. 10.1016/j.jprot.2008.05.004 · DOI
  89. 2016, Membrane-bound electron transport systems of an anammox bacterium: A complexome analysis, Biochim. Biophys. Acta - Bioenerg, 1857, 1694, 10.1016/j.bbabio.2016.07.006 · DOI
  90. 2021, Investigation of central energy metabolism-related protein complexes of ANME-2d methanotrophic archaea by complexome profiling, BBA - Bioenerg, 1862, 148308, 10.1016/j.bbabio.2020.148308 · DOI
  91. 10.1016/0003-2697(87)90587-2 · DOI
  92. Schägger, H. Tricine-SDS-PAGE. Nat. Protoc. 1, (2006). · DOI
  93. 10.1038/nprot.2007.261 · DOI · Paper page
  94. Tyanova, S. , Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry–based shotgun proteomics. Nat. Protoc. 11, (2016). · DOI
  95. 2021, MS Annika: A New Cross-Linking Search Engine, J. Proteome Res, 20, 2560, 10.1021/acs.jproteome.0c01000 · DOI
  96. 10.1038/s41596-018-0068-8 · DOI
  97. 10.1074/mcp.M116.058560 · DOI
  98. 2017, MSFragger: Ultrafast and comprehensive peptide identification in mass spectrometry-based proteomics, Nat. Methods, 14, 513, 10.1038/nmeth.4256 · DOI
  99. 10.1038/s41587-019-0201-4 · DOI · Paper page
  100. 10.1093/bioinformatics/btt656 · DOI · Paper page
  101. 2021, Community-led, integrated, reproducible multi-omics with anvi’o, Nat. Microbiol, 6, 3, 10.1038/s41564-020-00834-3 · DOI
  102. 10.1093/bioinformatics/btp348 · DOI
  103. 10.1038/s41587-019-0036-z · DOI
  104. 10.1093/nar/gky1106 · DOI
  105. 10.1093/bioinformatics/btu531 · DOI
  106. 10.1093/nar/28.1.235 · DOI · Paper page

Metadata

Authors
Hodgskiss, L. H., Melcher, M., Kerou, M., Chen, W., Ponce-Toledo, R. I., Savvides, S. N., Wienkoop, S., Hartl, M., & Schleper, C.
Affiliations
  • University of Vienna (AT)
  • Vlaams Instituut voor Biotechnologie (BE)
Corresponding author
Schleper, Christa
ORCID
Venue
The ISME Journal
Publisher
openRxiv
Published
2022-04-06
Volume
17
Issue
4
Pages
588-599
ISSN
1751-7362 (ISSN-L)
DOI
10.1101/2022.04.06.487334
PMC
PMC10030591
OpenAlex
W4318700676
Cited by
58
References
1
Citations by year
2026: 17 · 2025: 16 · 2024: 12 · 2023: 12 · 2022: 1
FWCI
5.08
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • The ISME Journal (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
Funders
  • European Commission (2021–2027, 101079299)
  • Austrian Science Fund (W1257)
  • Universität Wien
  • H2020 European Research Council (695192)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
  • Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
  • Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
Keywords
ammonia monooxygenase, ammonia-oxidizing archaea, nitrification, Xiamen, enzyme subunit composition, particulate methane monooxygenase, extracellular domain, nitrogen cycling
MeSH terms
Ammonia, Archaea, Oxidation-Reduction, Oxidoreductases, Phylogeny, Soil Microbiology, Gene Expression, Nitrification, Native Polyacrylamide Gel Electrophoresis

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