Brief report
Nitric oxide reductase (norB) gene sequence analysis
reveals discrepancies with nitrite reductase (nir) gene
phylogeny in cultivated denitrifiers
Kim Heylen,
1
* Bram Vanparys,
1
Dirk Gevers,
1,2
Lieven Wittebolle,
3
Nico Boon
3
and Paul De Vos
1
1
Laboratory of Microbiology, Department of
Biochemistry, Physiology and Microbiology, Ghent
University, K.L. Ledeganckstraat 35, B-9000 Gent,
Belgium.
2
Bioinformatics and Evolutionary Genomics, Ghent
University/VIB, Technologiepark 927, B-9052 Gent,
Belgium.
3
Laboratory of Microbial Ecology and Technology
(LabMET), Ghent University, Coupure Links 653,
B-9000 Gent, Belgium.
Summary
Gene sequence analysis of cnorB and qnorB, both
encoding nitric oxide reductases, was performed on
pure cultures of denitrifiers, for which previously nir
genes were analysed. Only 30% of the 227 denitrifying
strains rendered a norB amplicon. The cnorB gene
was dominant in Alphaproteobacteria, and domi-
nantly coexisted with the nirK gene, coding for the
copper-containing nitrite reductase. Both norB genes
were equally present in Betaproteobacteria but no
linked distributional pattern of nir and norB genes
could be observed. The overall cnorB phylogeny was
not congruent with the widely accepted organism
phylogeny based on 16S rRNA gene sequence analy-
sis, with strains from different bacterial classes
having identical cnorB sequences. Denitrifiers and
non-denitrifiers could be distinguished through
qnorB gene phylogeny, without further grouping at a
higher taxonomic resolution. Comparison of nir and
norB phylogeny revealed that genetic linkage of both
genes is not widespread among denitrifiers. Thus,
independent evolution of the genes for both nitrogen
oxide reductases does also occur.
Introduction
Nitric oxide (NO) in excess is toxic to bacteria, fungi,
microbial parasites, tumour cells and viruses, because it
can damage DNA, proteins and lipids. The detoxification
of NO through reduction is innate to denitrifiers, which
catalyse the sequential dissimilatory reduction of nitrate to
nitrite, and further via NO to N
2O and N2 under oxygen-
limited conditions. Non-denitrifying, mostly pathogenic
strains can also contain a NO reductase, which is advan-
tageous in the survival in oxygen-limited environments
and confers protection against exogenous and endog-
enous nitrosative stress (Philippot, 2005).
Three nitric oxide reductases have been described to
date. The best described is the membrane-bound dimer
NORCB. All bacterial strains found with this nitric oxide
reductase, designated NORB, cNORB or short-chain
NOR (scNOR), could perform denitrification (Bartnikas
et al., 1997; Philippot et al., 2001; Braker and Tiedje,
2003; Chan and McCormick, 2004). A second, single-
component nitric oxide reductase has an N-terminal
extension coding for quinol as electron donor and two-
thirds of the catalytic region show homology with cNORB
(Cramm et al., 1997). This nitric oxide reductase is termed
qNORB, NORZ or long-chain NOR (lcNOR). The qnorB
gene has been found to date in both denitrifiers and
non-denitrifying strains (Cramm et al., 1999; Büsch et al.,
2002; Philippot, 2005). A third nitric oxide reductase, puri-
fied from Bacillus azotoformans, uses menaquinol as
electron acceptor (Suharti and de Vries, 2005). The genes
encoding this menaquinol nitric oxide reductase are hith-
erto unknown.
Because denitrifiers are not a monophyletic group of
bacteria (Knowles, 1982; Tiedje, 1988), cultivation-
independent studies on the denitrifying communities in
the environment use the genes targeting the key enzymes
of denitrification, nirS or nirK coding for nitrite reductase
(Braker et al., 2000; Priemé et al., 2002; Yan et al., 2003;
Yoshie et al., 2004; Sharma et al., 2005) and/or norB
coding for nitric oxide reductase (Braker and Tiedje, 2003;
Casciotti and Ward, 2005). However, cultivation-based
Received 13 October, 2006; accepted 18 October, 2006. *For
correspondence. E-mail Kim.Heylen@UGent.be; Tel. (+32)
92645101; Fax (+32) 92645092.
Environmental Microbiology (2007) 9(4), 1072–1077 doi:10.1111/j.1462-2920.2006.01194.x
© 2006 Ghent University
Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd