Isolation of 'Candidatus Nitrosocosmicus franklandus', a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration

Laura E. Lehtovirta-Morley; Jenna Ross; Linda Hink; Eva B. Weber; Cécile Gubry-Rangin; Cécile Thion; James I. Prosser; Graeme W. Nicol

doi:10.1093/femsec/fiw057

Isolation of 'Candidatus Nitrosocosmicus franklandus', a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration

Laura E. Lehtovirta-Morley, Jenna Ross, Linda Hink, Eva B. Weber, Cécile Gubry-Rangin, Cécile Thion, James I. Prosser, Graeme W. Nicol

University of Aberdeen

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Abstract

Studies of the distribution of ammonia oxidising archaea (AOA) and bacteria (AOB) suggest distinct ecological niches characterised by ammonia concentration and pH, arising through differences in substrate affinity and ammonia tolerance. AOA form five distinct phylogenetic clades, one of which, the 'Nitrososphaera sister cluster', has no cultivated isolate. A representative of this cluster, named 'Candidatus Nitrosocosmicus franklandus', was isolated from a pH 7.5 arable soil and we propose a new cluster name: 'Nitrosocosmicus'. While phylogenetic analysis of amoA genes indicates its association with the Nitrososphaera sister cluster, analysis of 16S rRNA genes provided no support for a relative branching that is consistent with a 'sister cluster', indicating placement within a lineage of the order Nitrososphaerales. 'Ca. N. franklandus' is capable of ureolytic growth and its tolerances to nitrite and ammonia are higher than in other AOA and similar to those of typical soil AOB. Similarity of other growth characteristics of 'Ca. N. franklandus' with those of typical soil AOB isolates reduces support for niche differentiation between soil AOA and AOB and suggests that AOA have a wider physiological diversity than previously suspected. In particular, the high ammonia tolerance of 'Ca. N. franklandus' suggests potential contributions to nitrification in fertilised soils.

Original language	English
Article number	fiw057
Pages (from-to)	1-10
Number of pages	10
Journal	FEMS Microbiology Ecology
Volume	92
Issue number	5
Early online date	13 Mar 2016
DOIs	https://doi.org/10.1093/femsec/fiw057
Publication status	Published - May 2016

Bibliographical note

Acknowledgements
The authors would like to thank Mr Kevin Mackenzie and Mrs Gillian Milne (University of Aberdeen) for technical support with scanning electron microscopy, and Dr Robin Walker for access to the Woodlands Field experimental plots at the SRUC,Craibstone Estate, Aberdeen.

Funding
This work was financially supported by Natural Environmental Research Council (standard grants NE/I027835/1 and NE/L006286/1 and fellowship NE/J019151/1), EC Marie Curie ITN NORA, Grant Agreement No. 316472, the AXA Research Fund and the Centre for Genome Enabled Biology and Medicine, University of Aberdeen.

Keywords

thaumarchaeota
nitrososphaera sister cluster
soil
ammonia inhibition
nitrosocosmicus
nitrification

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Isolation of ‘Candidatus Nitrosocosmicus franklandus’, a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration
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Cite this

Lehtovirta-Morley, L. E., Ross, J., Hink, L., Weber, E. B., Gubry-Rangin, C., Thion, C., Prosser, J. I., & Nicol, G. W. (2016). Isolation of 'Candidatus Nitrosocosmicus franklandus', a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration. FEMS Microbiology Ecology, 92(5), 1-10. Article fiw057. https://doi.org/10.1093/femsec/fiw057

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abstract = "Studies of the distribution of ammonia oxidising archaea (AOA) and bacteria (AOB) suggest distinct ecological niches characterised by ammonia concentration and pH, arising through differences in substrate affinity and ammonia tolerance. AOA form five distinct phylogenetic clades, one of which, the 'Nitrososphaera sister cluster', has no cultivated isolate. A representative of this cluster, named 'Candidatus Nitrosocosmicus franklandus', was isolated from a pH 7.5 arable soil and we propose a new cluster name: 'Nitrosocosmicus'. While phylogenetic analysis of amoA genes indicates its association with the Nitrososphaera sister cluster, analysis of 16S rRNA genes provided no support for a relative branching that is consistent with a 'sister cluster', indicating placement within a lineage of the order Nitrososphaerales. 'Ca. N. franklandus' is capable of ureolytic growth and its tolerances to nitrite and ammonia are higher than in other AOA and similar to those of typical soil AOB. Similarity of other growth characteristics of 'Ca. N. franklandus' with those of typical soil AOB isolates reduces support for niche differentiation between soil AOA and AOB and suggests that AOA have a wider physiological diversity than previously suspected. In particular, the high ammonia tolerance of 'Ca. N. franklandus' suggests potential contributions to nitrification in fertilised soils.",

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note = "Acknowledgements The authors would like to thank Mr Kevin Mackenzie and Mrs Gillian Milne (University of Aberdeen) for technical support with scanning electron microscopy, and Dr Robin Walker for access to the Woodlands Field experimental plots at the SRUC,Craibstone Estate, Aberdeen. Funding This work was financially supported by Natural Environmental Research Council (standard grants NE/I027835/1 and NE/L006286/1 and fellowship NE/J019151/1), EC Marie Curie ITN NORA, Grant Agreement No. 316472, the AXA Research Fund and the Centre for Genome Enabled Biology and Medicine, University of Aberdeen.",

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AU - Hink, Linda

AU - Weber, Eva B.

AU - Gubry-Rangin, Cécile

AU - Thion, Cécile

AU - Prosser, James I.

AU - Nicol, Graeme W.

N1 - Acknowledgements The authors would like to thank Mr Kevin Mackenzie and Mrs Gillian Milne (University of Aberdeen) for technical support with scanning electron microscopy, and Dr Robin Walker for access to the Woodlands Field experimental plots at the SRUC,Craibstone Estate, Aberdeen. Funding This work was financially supported by Natural Environmental Research Council (standard grants NE/I027835/1 and NE/L006286/1 and fellowship NE/J019151/1), EC Marie Curie ITN NORA, Grant Agreement No. 316472, the AXA Research Fund and the Centre for Genome Enabled Biology and Medicine, University of Aberdeen.

PY - 2016/5

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N2 - Studies of the distribution of ammonia oxidising archaea (AOA) and bacteria (AOB) suggest distinct ecological niches characterised by ammonia concentration and pH, arising through differences in substrate affinity and ammonia tolerance. AOA form five distinct phylogenetic clades, one of which, the 'Nitrososphaera sister cluster', has no cultivated isolate. A representative of this cluster, named 'Candidatus Nitrosocosmicus franklandus', was isolated from a pH 7.5 arable soil and we propose a new cluster name: 'Nitrosocosmicus'. While phylogenetic analysis of amoA genes indicates its association with the Nitrososphaera sister cluster, analysis of 16S rRNA genes provided no support for a relative branching that is consistent with a 'sister cluster', indicating placement within a lineage of the order Nitrososphaerales. 'Ca. N. franklandus' is capable of ureolytic growth and its tolerances to nitrite and ammonia are higher than in other AOA and similar to those of typical soil AOB. Similarity of other growth characteristics of 'Ca. N. franklandus' with those of typical soil AOB isolates reduces support for niche differentiation between soil AOA and AOB and suggests that AOA have a wider physiological diversity than previously suspected. In particular, the high ammonia tolerance of 'Ca. N. franklandus' suggests potential contributions to nitrification in fertilised soils.

AB - Studies of the distribution of ammonia oxidising archaea (AOA) and bacteria (AOB) suggest distinct ecological niches characterised by ammonia concentration and pH, arising through differences in substrate affinity and ammonia tolerance. AOA form five distinct phylogenetic clades, one of which, the 'Nitrososphaera sister cluster', has no cultivated isolate. A representative of this cluster, named 'Candidatus Nitrosocosmicus franklandus', was isolated from a pH 7.5 arable soil and we propose a new cluster name: 'Nitrosocosmicus'. While phylogenetic analysis of amoA genes indicates its association with the Nitrososphaera sister cluster, analysis of 16S rRNA genes provided no support for a relative branching that is consistent with a 'sister cluster', indicating placement within a lineage of the order Nitrososphaerales. 'Ca. N. franklandus' is capable of ureolytic growth and its tolerances to nitrite and ammonia are higher than in other AOA and similar to those of typical soil AOB. Similarity of other growth characteristics of 'Ca. N. franklandus' with those of typical soil AOB isolates reduces support for niche differentiation between soil AOA and AOB and suggests that AOA have a wider physiological diversity than previously suspected. In particular, the high ammonia tolerance of 'Ca. N. franklandus' suggests potential contributions to nitrification in fertilised soils.

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DO - 10.1093/femsec/fiw057

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M1 - fiw057

ER -

Isolation of 'Candidatus Nitrosocosmicus franklandus', a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration

Abstract

Bibliographical note

Keywords

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