Dynamics and functional relevance of
ammonia-oxidizing archaea in two agricultural soils
Kristina Schauss,
1†
Andreas Focks,
2†
Sven Leininger,
3†
Anja Kotzerke,
4
Holger Heuer,
5
Sören Thiele-Bruhn,
6
Shilpi Sharma,
1
Berndt-Michael Wilke,
4
Michael Matthies,
2
Kornelia Smalla,
5
Jean Charles Munch,
1
Wulf Amelung,
7
Martin Kaupenjohann,
8
Michael Schloter
1
*
†
and Christa Schleper
3
**
†‡
1
Helmholtz Zentrum München, German Research
Center for Environmental Health, Institute for Soil
Ecology, Ingolstädter Landstr. 1, 85764 Neuherberg,
Germany.
2
University of Osnabrück, Institute of Environmental
Systems Research, Barbarastr. 12, 49069 Osnabrück,
Germany.
3
University of Bergen, Institute for Biology, Jahnebakken
5, 5020 Bergen, Norway.
4
Berlin University of Technology, Institute of Ecology,
Franklinstr. 29, 10587 Berlin, Germany.
5
Julius Kühn Institute, Federal Research Centre for
Cultivated Plants, Institute for Epidemiology and
Pathogen Diagnostics, Messeweg 11-12, 38104
Braunschweig, Germany.
6
University of Trier, Department of Soil Science,
Behringstr. 21, 54286 Trier, Germany.
7
University of Bonn, Institute of Crop Science and
Resource Conservation – Soil Science and Soil
Ecology, Nussallee 13, 53115 Bonn, Germany.
8
Berlin University of Technology, Institute of Ecology,
Salzufer 11-12, 10587 Berlin, Germany.
Summary
Crucial steps in geochemical cycles are in many cases
performed by more than one group of microorgan-
isms, but the significance of this functional redun-
dancy with respect to ecosystem functioning is poorly
understood. Ammonia-oxidizing archaea (AOA) and
their bacterial counterparts (AOB) are a perfect system
to address this question: although performing the
same transformation step, they belong to well-
separated phylogenetic groups. Using pig manure
amended with different concentrations of sulfadiazine
(SDZ), an antibiotic that is frequently used in veteri-
nary medicine, it was possible to affect AOB and AOA
to different degrees. Addition of manure stimulated
growth of AOB in both soils and, interestingly, also
growth of AOA was considerably stimulated in one of
the soils. The antibiotic treatments decreased the
manure effect notably on AOB, whereas AOA were
affected to a lower extent. Model calculations concern-
ing the respective proportions of AOA and AOB in
ammonia oxidation indicate a substantial contribution
of AOA in one of the soils that further increased under
the influence of SDZ, hence indicating functional
redundancy between AOA and AOB.
Introduction
Microbial communities in terrestrial environments are
extremely complex, both with respect to their phylogeny
and with respect to their physiology (Gans et al., 2005;
O’Donnell et al., 2007). However, the significance of this
diversity for stability and functioning of these ecosystems
remains poorly understood (Prosser et al., 2007). The
application of models in soil microbial ecology combining
process data and abundance data of functional groups
has been suggested to address such questions (Rittmann
et al., 2006; Prosser et al., 2007), but has been rarely
applied so far (Garnier et al., 2003; Dassonville et al.,
2004; Khalil et al., 2005).
Oxidation of ammonia, which is the first step in nitrifi-
cation, a key process in the global nitrogen cycle resulting
in the formation of nitrate, is an interesting process to be
studied in this respect. Despite the huge phylogenetic and
physiological diversity that is found in the two domains of
bacteria and archaea, only a few selected groups seem to
be able to transform ammonia into nitrite. Therefore, this
step has been described as ‘pinhole’ in microbial nitrogen
turnover. For almost five decades two specific groups of
b- and g-proteobacteria have been considered as most
important contributors to ammonia oxidation (Bock and
Wagner, 2006). However recently, ammonia oxidizers of
the domain archaea were identified through metagenomic
and cultivation studies from terrestrial and marine
ecosystems (Könneke et al., 2005; Schleper et al., 2005;
Treusch et al., 2005; Hallam et al., 2006). Quantification
Received 14 December, 2007; accepted 23 August, 2008. For corre-
spondence. *E-mail schloter@gsf.de; Tel. (+49) 89 3178 2304;
Fax (+49) 89 3178 3376; **E-mail christa.schleper@univie.ac.at; Tel.
(+43) 1 4277 57320; Fax (+43) 1 4277 9578.
†
These authors contrib-
uted equally to this work.
‡
Present address: University of Vienna,
Faculty of Life Sciences, Althanstr. 14, A-1090 Vienna, Austria.
Environmental Microbiology (2009) 11(2), 446–456 doi:10.1111/j.1462-2920.2008.01783.x
© 2008 The Authors
Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd