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

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.

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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.

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Correspondence to Annette Bollmann.

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Sedlacek, C.J., McGowan, B., Suwa, Y. et al. A Physiological and Genomic Comparison of Nitrosomonas Cluster 6a and 7 Ammonia-Oxidizing Bacteria. Microb Ecol 78, 985–994 (2019). https://doi.org/10.1007/s00248-019-01378-8

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Keywords

  • Ammonia-oxidizing bacteria
  • Nitrosomonas
  • Nitrification
  • Niche differentiation
  • Ammonium availability