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Cited by 45Wastewater Treatment and Nitrogen RemovalMicrobial metabolism and enzyme functionMicrobial Community Ecology and Physiology

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Ecophysiology and Comparative Genomics of Nitrosomonas mobilis Ms1 Isolated from Autotrophic Nitrifying Granules of Wastewater Treatment Bioreactor

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Thandar, Soe Myat, Ushiki, Norisuke, Fujitani, Hirotsugu, Sekiguchi, Yuji, Tsuneda, Satoshi·2016·Frontiers in Microbiology
DOI 10.3389/fmicb.2016.01869PMC PMC5118430
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Abstract

Ammonia-oxidizing bacteria (AOB), which oxidize ammonia to nitrite in the first step of nitrification, play an important role in biological wastewater treatment systems. Nitrosomonas mobilis is an important and dominant AOB in various wastewater treatment systems. However, the detailed physiological and genomic properties of N. mobilis have not been thoroughly investigated because of limited success isolating pure cultures. This study investigated the key physiological characteristics of N. mobilis Ms1, which was previously isolated into pure culture from the nitrifying granules of wastewater treatment bioreactor. The pure culture of N. mobilis Ms1 was cultivated in liquid mineral medium with 30 mg-N L-1 (2.14 mM) of ammonium at room temperature under dark conditions. The optimum growth of N. mobilis Ms1 occurred at 27°C and pH 8, with a maximum growth rate of 0.05–0.07 h-1, which corresponded to a generation time of 10–14 h. The half saturation constant for ammonium uptake rate and the maximum ammonium uptake rate of N. mobilis Ms1 were 30.70±0.51 μM NH4+ and 0.01±0.002 pmol NH4+ cells-1 h-1, respectively. N. mobilis Ms1 had higher ammonia oxidation activity than N. europaea in this study. The oxygen uptake activity kinetics of N. mobilis Ms1 were K_(m(O_2))= 21.74±4.01 μM O2 and V_(max⁡(O_2))= 0.06±0.02 pmol O2 cells-1 h-1. Ms1 grew well at ammonium and NaCl concentrations of up to 100 mM and 500 mM, respectively. The nitrite tolerance of N. mobilis Ms1 was extremely high (up to 300 mM) compared to AOB previously isolated from activated sludge and wastewater treatment plants. The average nucleotide identity between the genomes of N. mobilis Ms1 and other Nitrosomonas species indicated that N. mobilis Ms1 was distantly related to other Nitrosomonas species. The organization of the genes encoding protein inventory involved in ammonia oxidation and nitrifier denitrification processes were different from other Nitrosomonas species. The current study provides a needed physiological and genomic characterization of N. mobilis-like bacteria and a better understanding of their ecophysiological properties, enabling comparison of these bacteria with other AOB in wastewater treatment systems and natural ecosystems.

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FIGURE 1 Effect of temperature, pH and NaCl concentration on the growth of N. mobilis Ms1. The nitrite concentrations of N. mobilis Ms1 after 24 h of incubation at different temperatures (A), pHs (B), and NaCl concentrations (C). Bars are the standard errors (n = 3).
FIGURE 1 Effect of temperature, pH and NaCl concentration on the growth of N. mobilis Ms1. The nitrite concentrations of N. mobilis Ms1 after 24 h of incubation at different temperatures (A), pHs (B), and NaCl concentrations (C). Bars are the standard errors (n = 3).CC BY · PubMed Central
FIGURE 2 Growth of N. mobilis Ms1 determined by measurement of time courses of ammonium concentrations (triangle), nitrite concentrations (circle) and cell numbers (rectangle) during incubation for 5 days. The maximum growth rate calculated from the increased number of cells was observed on days 3 and 4 (open rectangle).
FIGURE 2 Growth of N. mobilis Ms1 determined by measurement of time courses of ammonium concentrations (triangle), nitrite concentrations (circle) and cell numbers (rectangle) during incubation for 5 days. The maximum growth rate calculated from the increased number of cells was observed on days 3 and 4 (open rectangle).CC BY · PubMed Central
FIGURE 3 Representative data describing ammonium uptake activities of N. mobilis Ms1 and N. europaea. The best-fit curve was described according to the Michaelis–Menten equation to obtain Km (NH4⁺) and V max (NH4⁺) values.
FIGURE 3 Representative data describing ammonium uptake activities of N. mobilis Ms1 and N. europaea. The best-fit curve was described according to the Michaelis–Menten equation to obtain Km (NH4⁺) and V max (NH4⁺) values.CC BY · PubMed Central
FIGURE 4 Representative data describing oxygen uptake of N. mobilis Ms1. The best-fit curve was described according to the Michaelis–Menten equation to obtain Km (O2) and Vmax (O2) values.
FIGURE 4 Representative data describing oxygen uptake of N. mobilis Ms1. The best-fit curve was described according to the Michaelis–Menten equation to obtain Km (O2) and Vmax (O2) values.CC BY · PubMed Central
FIGURE 5 Ammonium and nitrite tolerance of N. mobilis Ms1. (A) Maximum produced nitrite concentration rate per day of N. mobilis Ms1 incubation with different initial ammonium concentrations (10, 50, 100, 200, 300, 400, and 500 mM). (B) Maximum ammonia oxidation rate per day of N. mobilis Ms1 incubation with different initial nitrite concentrations (0, 5, 10, 50, 100, 200, 300, 400, and 500 mM) under 5 mM initial ammonium concentration. Bars are the standard errors (n = 2).
FIGURE 5 Ammonium and nitrite tolerance of N. mobilis Ms1. (A) Maximum produced nitrite concentration rate per day of N. mobilis Ms1 incubation with different initial ammonium concentrations (10, 50, 100, 200, 300, 400, and 500 mM). (B) Maximum ammonia oxidation rate per day of N. mobilis Ms1 incubation with different initial nitrite concentrations (0, 5, 10, 50, 100, 200, 300, 400, and 500 mM) under 5 mM initial ammonium concentration. Bars are the standard errors (n = 2).CC BY · PubMed Central
FIGURE 6 Organization of the cluster of genes involved in the ammonia oxidation of N. mobilis Ms1. (A) Cluster of genes encoding ammonia monooxygenase; NSMM_350046, the length of 159 bp, is the gene encoding protein with unknown function (B) cluster of genes encoding hydroxylamine oxidoreductase and associated cytochromes. The separate fragments haoA3, haoA4, cycA3, and cycA4, with the sequence length of 117, 165, 108, and 129 bp, respectively, were shorter than their respective version in the operon, and these were located at the end of the contigs and 3′ ends of the haoA3 and haoA4, and 5′ ends of the cycA3 and cycA4 were not included in the sequence of the contigs.
FIGURE 6 Organization of the cluster of genes involved in the ammonia oxidation of N. mobilis Ms1. (A) Cluster of genes encoding ammonia monooxygenase; NSMM_350046, the length of 159 bp, is the gene encoding protein with unknown function (B) cluster of genes encoding hydroxylamine oxidoreductase and associated cytochromes. The separate fragments haoA3, haoA4, cycA3, and cycA4, with the sequence length of 117, 165, 108, and 129 bp, respectively, were shorter than their respective version in the operon, and these were located at the end of the contigs and 3′ ends of the haoA3 and haoA4, and 5′ ends of the cycA3 and cycA4 were not included in the sequence of the contigs.CC BY · PubMed Central

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Metadata

Authors
Thandar, S. M., Ushiki, N., Fujitani, H., Sekiguchi, Y., & Tsuneda, S.
Affiliations
  • Mandalay Technological University (MM)
  • Waseda University (JP)
  • National Institute of Advanced Industrial Science and Technology (JP)
Corresponding author
Tsuneda, Satoshi
ORCID
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2016-11-22
Volume
7
Pages
1869-1869
ISSN
1664-302X (ISSN-L)
DOI
10.3389/fmicb.2016.01869
PMC
PMC5118430
OpenAlex
W2553323154
Cited by
45
References
54
Citations by year
2026: 5 · 2025: 6 · 2024: 9 · 2023: 2 · 2022: 5 · 2021: 8 · 2020: 5 · 2019: 2 · 2018: 3
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Institute for Fermentation, Osaka
  • Waseda University (2014B-323)
  • Tokyo University of Agriculture
Topics
  • Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
ammonia-oxidizing bacteria, nitrification, pure culture isolation, growth kinetics, oxygen uptake kinetics, nitrite tolerance, salt tolerance, average nucleotide identity, comparative genomics, Nitrosomonas europaea

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Thandar, S. M., Ushiki, N., Fujitani, H., Sekiguchi, Y., & Tsuneda, S. (2016). Ecophysiology and Comparative Genomics of Nitrosomonas mobilis Ms1 Isolated from Autotrophic Nitrifying Granules of Wastewater Treatment Bioreactor. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2016.01869