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A Physiological and Genomic Comparison of Nitrosomonas Cluster 6a and 7 Ammonia-Oxidizing Bacteria

  • Christopher J. Sedlacek
  • Brian McGowan
  • Yuichi Suwa
  • Luis Sayavedra-Soto
  • Hendrikus J. Laanbroek
  • Lisa Y. Stein
  • Jeanette M. Norton
  • Martin G. Klotz
  • Annette BollmannEmail author
Genes and Genomes

Abstract

Ammonia-oxidizing bacteria (AOB) within the genus Nitrosomonas perform the first step in nitrification, ammonia oxidation, and are found in diverse aquatic and terrestrial environments. Nitrosomonas AOB were grouped into six defined clusters, which correlate with physiological characteristics that contribute to adaptations to a variety of abiotic environmental factors. A fundamental physiological trait differentiating Nitrosomonas AOB is the adaptation to either low (cluster 6a) or high (cluster 7) ammonium concentrations. Here, we present physiological growth studies and genome analysis of Nitrosomonas cluster 6a and 7 AOB. Cluster 6a AOB displayed maximum growth rates at ≤ 1 mM ammonium, while cluster 7 AOB had maximum growth rates at ≥ 5 mM ammonium. In addition, cluster 7 AOB were more tolerant of high initial ammonium and nitrite concentrations than cluster 6a AOB. Cluster 6a AOB were completely inhibited by an initial nitrite concentration of 5 mM. Genomic comparisons were used to link genomic traits to observed physiological adaptations. Cluster 7 AOB encode a suite of genes related to nitrogen oxide detoxification and multiple terminal oxidases, which are absent in cluster 6a AOB. Cluster 6a AOB possess two distinct forms of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and select species encode genes for hydrogen or urea utilization. Several, but not all, cluster 6a AOB can utilize urea as a source of ammonium. Hence, although Nitrosomonas cluster 6a and 7 AOB have the capacity to fulfill the same functional role in microbial communities, i.e., ammonia oxidation, differentiating species-specific and cluster-conserved adaptations is crucial in understanding how AOB community succession can affect overall ecosystem function.

Keywords

Ammonia-oxidizing bacteria Nitrosomonas Nitrification Niche differentiation Ammonium availability 

Notes

Acknowledgements

We thank the Center for Genome Research and Biocomputing (CGRB) at Oregon State University for the sequencing services, the Center for Bioinformatics and Functional Genomics at Miami University for access to CLC workbench, and Dr. Petra Pjevac for assistance with phylogenomics.

Funding

This work was funded by start-up funds from Miami University to A Bollmann, a National Science Foundation grant (DEB-1120443) to A Bollmann, a NSF Research Coordination Network grant 0541797 (Nitrification) to DJ Arp, WJ Hickey, MG Klotz, JM Norton, and BB Ward, Miami University Undergraduate Research Awards to B McGowan, and Utah Agricultural Experiment Station, Utah State University to JM Norton.

Supplementary material

248_2019_1378_MOESM1_ESM.docx (36 kb)
Supplementary Table 1 (DOCX 35 kb)
248_2019_1378_MOESM2_ESM.docx (13 kb)
Supplementary Table 2 (DOCX 13 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Christopher J. Sedlacek
    • 1
    • 2
  • Brian McGowan
    • 1
  • Yuichi Suwa
    • 3
  • Luis Sayavedra-Soto
    • 4
  • Hendrikus J. Laanbroek
    • 5
  • Lisa Y. Stein
    • 6
  • Jeanette M. Norton
    • 7
  • Martin G. Klotz
    • 8
  • Annette Bollmann
    • 1
    Email author
  1. 1.Department of MicrobiologyMiami UniversityOxfordUSA
  2. 2.Department of Microbiology and Ecosystem Science, Division of Microbial EcologyUniversity of ViennaViennaAustria
  3. 3.Department of Biological SciencesChuo UniversityTokyoJapan
  4. 4.Department of Botany and Plant PathologyOregon State UniversityCorvallisUSA
  5. 5.Department of Microbial EcologyNetherlands Institute of EcologyWageningenThe Netherlands
  6. 6.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  7. 7.Department of Plants, Soil and ClimateUtah State UniversityLoganUSA
  8. 8.School of Molecular BiosciencesWashington State UniversityRichlandUSA

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