Biochemical Society Transactions (2011) Volume 39, part 1
SUPPLEMENTARY ONLINE DATA
Denitrification in Gram-positive bacteria: an
underexplored trait
Ines Verbaendert*, Paul De Vos*†, Nico Boon‡ and Kim Heylen*1
www.biochemsoctrans.org
*Laboratory of Microbiology (LM-UGent), Department of Biochemistry and Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent, Belgium,
†BCCM/LMG Bacteria Collection, Laboratory of Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent, Belgium, and ‡Laboratory of Microbial
Ecology (LabMET), Ghent University, Coupure Links 653, 9000 Gent, Belgium
Table S1 Overview of Gram-positive bacteria once claimed to denitrify and current status of their denitrification capacity
This Table is an updated heuristic annotated list of strains that denitrify, or were once claimed to, how denitrification was assessed and the current
√
status of our knowledge of their denitrification ability. Denitrification status is given as , denitrification; − , no denitrification; ?, not clear.
(a) (Endo)spore-forming Gram-positive bacteria: Bacillales
Species
Denitrification assessment
Current status
Anoxybacillus pushinoensis (AT-1 and AT-2) [1]
Presence of NO3 − was tested using a
More recent literature not available
√
modified Griess reagent, gas samples
from the head space were analysed
with gas chromatography.
Observations: ability to reduce NO3 −
and NO2 − , >99 % of the
composition of the gases was N2
Bacillus azotoformans (CIP R925) [2,3]
Isolation by N2 O enrichment; NO3 − ,
NO2 − and N2 O were used
anaerobically, considerable quantities
of N2 were produced during
reduction of NO3 − , NO2 − and N2 O;
Biochemical Society Transactions
Status
Purification and biochemical
characterization of qCuA NOR of
Bacillus azotoformans (NCCB
√
100003); the encoding genes are
not known yet [4–6].
NO3 − reductase, NO2 − reductase,
NO reductase and N2 O reductase
were present. Methods were not
Bacillus cereus (ATCC 8035) [7]
Bacillus circulans (no strain number) [8]
mentioned
Biochemical comparison of enzymatic
biosynthesis was performed.
Maximal denitrifying activity of
strains isolated from soddy
Observation: appearance of NO3 −
and NO2 − reductase activity in cell
suspensions from cells of anaerobic
podzolic soil has been determined
by gas chromatographic analysis
of N2 O evolved from NO3 − with
cultures
the acetylene inhibition method
(AIM) [8]. Bacillus cereus (PK-5) is
involved in aerobic denitrification
with conversion of NO3 − to N2
[9]
More recent literature not available
Observation: maximal denitrifying
√
√
activity was determined by AIM and
gas chromatographic analysis of N2 O
evolved from NO3 −
1
To whom correspondence should be addressed (email [email protected]).
C The
C 2011 Biochemical Society
Authors Journal compilation Biochem. Soc. Trans. (2011) 39, 254–258; doi:10.1042/BST0390254
Enzymology and Ecology of the Nitrogen Cycle
Table S1 (Continued)
Species
Denitrification assessment
Current status
Bacillus firmus (NIAS 237) [10]
Enzyme analysis was performed by cell fractionation
and proton translocation measurements.
Observation: dissimilatory NO2 − reductase was
More recent literature not
available
Bacillus licheniformis (multiple strains) [11]
located on the cytoplasmic membrane, its reducing
side was on the inner side of this membrane
NO2 − was analysed colorimetrically, identification
Bacillus licheniformis (PK-16) is
and measurement of NO, N2 O and N2 was
established by gas chromatography. Enzymatic
extracts were used to detect NO3 − and
Status
√
√
involved in aerobic
denitrification with conversion
of NO3 − into N2 [9]
NO2 − reductase activity. Observations: NO3 − and
NO reductase enzymes were detected in enzymatic
extracts, but not the NO2 − and N2 O reductases.
Bacillus nitritollens (multiple strains) [12]
N2 O and N2 production from NO3 − was slow and
weak
Simple phenotypic testing†: Observations: gas is
Recent literature not available
produced under anaerobic conditions, and NO2 − is
produced from NO3 − and it rapidly disappears
Bacillus subtilis (I-41) [13]
Nitrite concentration was studied with ion
chromatography, the presence of nitrate was
assayed by reducing nitrate with zinc powder. N2
These B. subtilis strains require
more detailed descriptions
−
√
and N2 O in the gaseous phase were analysed by
gas chromatography. Observations: significant
levels of N2 O and N2 were observed in the gas
Bacillus sp.
phase, NO2 − was reduced
Denitrification activity was screened for strain R22
after anaerobic growth with NO3 − as terminal
More recent literature not
available
√
electron acceptor, confirmed with AIM and N2 O
accumulation measured by gas chromatography.
nirS (AJ626841) gene sequenced [14]. For strain
R-13: nirS (AF335924) gene sequenced.
nirS-containing strains were tested for their ability
to remove NO3 − and NO2 − [15]. For strain
TSA4w: nirS (AB542306) gene sequenced. For
strain R-32546 and R-31856: nirK gene sequenced
(AM404294 and AM404293). For strains R-33773
(AM778674), R-32656 (AM778673), R-31770
(AM778672), R-31841 (AM778671), R-32702
(AM778670), R-33820 (AM778669), R-32709
(AM778667), R-32715 (AM404295), R-32526
(AM403579) and strain SH3–SH63 (EU374113 to
EU374135): qnorB genes sequenced. For strain
R-32694: qnorB and cnorB (AM778668, AM403581)
sequenced. Only gene information available on the
Brevibacillus ginsengisoli (Gsoil 3088T ) [16]
NCBI website (http://ncbi.nlm.nih.gov)
Anaerobic growth under ‘denitrifying conditions’ only
in the presence of NO3 − , with reduction of NO3 −
More recent literature not
available
−
to NO2 − . Only reduction of NO3 − was analysed;
what is meant by ‘denitrifying conditions’ is not
clear
C The
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Authors Journal compilation Biochemical Society Transactions (2011) Volume 39, part 1
Table S1 (Continued)
Species
Denitrification assessment
Current status
Status
Brevibacillus laterosporus (multiple strains)
[17]
Simple phenotypic testing† was performed.
Observations: reduction of NO3 − to NO2 −
and weak gas formation from NO3 − under
More recent literature not available
−
Genome encodes the cytochrome
bc-type NO reductase, norB [20],
?
Desulfitobacterium hafniense (DCB-2T and
PCP-1T ) [18,19]
anaerobic conditions
Only phenotypic reduction of NO3 − is tested,
NO3 − is reduced to NO2 −
it reveals a nosCZ · orf · nosDLFY
cluster and is predicted to encode
the Z-type N2 OR of Gram-negative
Enterococcus sp. (R-25205) [22]
NO3 − and NO2 − reduction tested with Griess
reagents in combination with presence of a
bacteria [21]
More recent literature not available
pH shift. Confirmation with gas
chromatography of N2 O and AIM. nirK
(AM230873) gene sequenced
Enterococcus sp. (R-24626) [22,23]
Nitrate and nitrite reduction tested with Griess
reagents in combination with presence of a
More recent literature not available
√
√
pH shift. Confirmation with gas
chromatography of N2 O and AIM. nirK
(AM230813) and cnorB (AM284330) genes
Geobacillus sp. (TDN01) [24]
sequenced
Reduction of NO3 − and NO2 − were
evaluated using the Griess–Romijn reagent
and ion chromatography, the amount of N2
and N2 O produced was analysed by gas
chromatography. Observation: production of
Geobacillus stearothermophilus (TnBA1)
[26]
N2 O and N2 gas from nitrate
N2 O and N2 were studied with Warburg
respirometry and gas chromatography
Further functional analysis of this
thermophilic denitrifying
bacterium was performed [25]
Description of the membrane-bound
denitrification enzymes of strain
using AIM. Enzyme activity was measured
for all nitrogenous reductases.
Observations: denitrification from NO2 − is
ATCC 12016, except N2 O
reductase [27]. No denitrification
in Geobacillus stearothermophilus
much faster than from NO3 − and the
process produces N2 O and N2
ATCC 12980T and DSM 22T
[28,29]. nirK and qnorB gene are
found in the genome of a
non-denitrifying G.
stearothermophilus strain [30]
Geobacillus subterraneus (strain Sam,
strain K, strain 34T ) [29]
Geobacillus thermodenitrificans (DSM
465T , DSM 466, strains TH6A, TH8A,
Occurrence of denitrification was measured
with gas chromatography. Observations:
anaerobic growth, reducing NO3 − and
NO2 − to N2
Reduction of NO3 − was examined with the
Griess reagent. NO3 − and NO2 − reduction
TH4B, TH45A, TH33A, TH35A, TH51A,
TH61A, BI5A, TU6F3) [28]
to gas and anaerobic production of gas
from NO3 − . Methods were not mentioned
More recent literature not available
Anaerobic growth of DSM 466,
reducing NO3 − and NO2 − to N2
(measurement with gas
chromatography) [29].
Identification of the genes for a
complete denitrification pathway
and a whole genome sequencing
approach yielded a complete
novel N2 O reductase gene in
strain NG80–2 [31], which was
functionally characterized [32]
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Authors Journal compilation √
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Enzymology and Ecology of the Nitrogen Cycle
Table S1 (Continued)
Species
Denitrification assessment
Current status
Geobacillus thermoleovorans (DSM 5366T )
[29]
Occurrence of denitrification was measured
with gas chromatography. The strain
grew anaerobically, reducing NO3 − to
No denitrification in strain DSM
5366T [28]
Paenibacillus larvae subsp. pulvifaciens
(multiple strains) [17]
N2
Simple phenotypic testing† was
performed. Observations: reduction of
NO3 − reduced to NO2 − ,
established by API test [33],
NO3 − to NO2 − and gas formation from
NO3 − under anaerobic conditions
Paenibacillus macerans (multiple strains)
[17]
Paenibacillus polymyxa (multiple strains)
[17]
Simple phenotypic testing† was performed.
Observations: reduction of NO3 − to
NO2 − and weak gas formation from
NO3 − under anaerobic conditions
Simple phenotypic testing† was performed.
Observations: reduction of NO3 − to
More recent literature not
available
Maximal denitrifying activity of
strains isolated from soddy
−
−
√
podzolic soil has been
determined by gas
chromatographic analysis of
N2 O evolved from NO3 − with
AIM [8]
Reduction of NO3 − and NO2 − to N2 or
N2 O under anaerobic culture conditions
was measured by the helium
√
but actual denitrification
capacity has not yet been
tested properly
NO2 − and weak gas formation from
NO3 − under anaerobic conditions
Paenibacillus spp. (multiple strains) [34]
Status
More recent literature not
available.
√
atmosphere incubation method.
Presence of functional genes coding for
nirK, nirS and nos was tested
Paenibacillus terrae (MH72 and AM141T )
[35]
Reduction of NO3 − to NO2 − and gas
chromatographic analysis of N2 and N2 O
Are the Paenibacillus terrae
strains fermentative or true
denitrifying strains?
?
Sporosarcina pasteurii [17]
Simple phenotypic testing† was performed.
Observations: reduction of NO3 − to
NO2 − and weak gas formation from
NO3 − reduction to NO2 − in
Sporosarcina [36]
−
Staphylococcus sp. (N23) [15]
NO3 − under anaerobic conditions
nirS-containing strains were tested for their
−
Staphylococcus sp. (R-25050) [22]
More recent literature not
−.
ability to remove NO3 and NO2 nirS
(AF335923) gene sequenced
NO3 − and NO2 − reduction tested with
available
More recent literature not
nirK (AM230813) gene sequenced
Gas chromatographic analysis of the
products of the denitrification reaction
√
available
Griess reagents in combination with the
presence of a pH shift. Confirmation with
gas chromatography of N2 O and AIM.
Virgibacillus halodenitrificans (ATCC 49067)
[37,38]
√
Growth occurs under anaerobic
conditions on marine agar, only
was performed. Observations: product of
denitrification is N2 O, the isolate lacks
N2 O reductase activity and NO3 − and
in the presence of NO3 − ,
which is reduced to NO2 −
[39]; no further specification of
NO2 − support anaerobic growth [37].
Purification of a copper-containing
NO2 − reductase [38]
denitrification
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Authors Journal compilation Biochemical Society Transactions (2011) Volume 39, part 1
Table S1 (Continued)
Species
Denitrification assessment
Current status
Status
Virgibacillus pantothenticus (multiple
strains) [17]
Simple phenotypic testing† was performed.
Observations: weak reduction of NO3 −
to NO2 − and weak gas formation from
NO3 − reduction to NO2 − (API
test) [40]. Growth occurs under
anaerobic conditions on marine
−
NO3 − under anaerobic conditions
agar, only in the presence of
NO3 − , which is reduced to
NO2 − [39]; no further
specification of denitrification
(b) (Endo)spore-forming Gram-positive bacteria: Actinomycetales
Species
Denitrification assessment
Current status
Status
More recent literature not
available
?
nirS (AF335922) gene sequenced.
Arthrobacter sp. (N6) [15]
nirS-containing strains were tested for their
ability to remove NO3 − and NO2 −
Denitrification was presumed positive if
neither NO2 − or NO3 − could be detected
or showed only traces in the supernatant
after isolate incubation. The final criteria for
considering an isolate a denitrifier were
detection of nirS or nirK by PCR followed by
BLAST sequence analysis. nirK (EU035283)
Arthrobacter sp. (61k) [41]
Arthrobacter sp. (TSA68)
gene sequenced
nirS (AB542303) gene sequenced. Only
More recent literature not
available
gene info available on the NCBI website
(http://ncbi.nlm.nih.gov)
N2 O in the gas phase was analysed by gas
√
?
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observation: N2 O
Dactylosporangium aurantiacum
(JCM 3041) [42]
evolution from both NO3 − and NO2 −
under O2 -limited conditions only
N2 O in the gas phase was analysed by gas
More recent literature not
available
√
More recent literature not
available
√
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observation: N2 O
Dermatophilus congolensis (JCM 3081) [42]
evolution from both NO3 − and NO2 −
under anaerobic and O2 -limited conditions
Screen for denitrification originated in a
number of denitrifying strains. N2 O in the
gas phase was analysed by gas
Frankia (no strain number) [43]
Kocuria varians (DN16) [44]
C The
C 2011 Biochemical Society
Authors Journal compilation chromatography and AIM
More recent literature not
available
Kocuria varians DN16 was
identified by GC-FAME as a
Nitrate and nitrite reduction tested with
Griess reagents, nirS, nirK and nosZ genes
member of the genus Kocuria,
but 16S rRNA analysis and BLAST
identified it as a member of the
amplified, nirS (AY345246) gene
sequenced
Gram-negative genus
Acinetobacter [44]
√
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Enzymology and Ecology of the Nitrogen Cycle
Table S1 (Continued)
Species
Denitrification assessment
Current status
Kineosporia aurantiaca (JCM 3230),
Nocardia salmonidica (JCM 4826),
Saccharomonospora caesia (JCM 3098)
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
More recent literature not
available
[42]
Microtetraspora glauca (JCM 3300) [42]
[15 N]nitrite tracers). Observation: N2 O
evolution from both NO3 − and NO2 − under
anaerobic and O2 -limited conditions
More recent literature not
available
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
Status
√
√
[15 N]nitrite tracers). Observations: N2 O
evolution from NO3 − under anaerobic
conditions and N2 O evolution from NO2 −
Pilimelia anulata (JCM 3090) [42]
under anaerobic and O2 -limited conditions
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
More recent literature not
available
√
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observation: N2 O
Saccharothrix australiensis (JCM 3370) [42]
evolution from both NO3 − and NO2 − under
anaerobic and O2 -limited conditions
N2 O in the gas phase was analysed by gas
More recent literature not
available
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observations: N2 O
evolution from both NO3 − and NO2 − under
O2 -limited conditions and N2 O evolution from
NO2 − under anaerobic conditions
Spirrilospora albida (JCM 3041) [42]
√
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
More recent literature not
available
√
[15 N]nitrite tracers). Observations: N2 O
evolution from NO2 − under anaerobic and
O2 -limited conditions and N2 O evolution from
Streptomyces akiyoshiensis (JCM 7970),
NO3 − under O2 -limited conditions
N2 O in the gas phase was analysed by gas
Isolation of denitrifying
Streptomyces aureofaciens (JCM 4624),
Streptomyces cavourensis subsp.
cavourensis (JCM 4555), Streptomyces
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observation: N2 O
Gram-positive Streptomyces
strains from a soil denitrifying
community [45], but the strains
cinnamoneus (JCM 4633), Streptomyces
coelicolor (JCM 4357), Streptomyces
endus (JCM 4636), Streptomyces glaucus
evolution from both NO3 − and NO2 − under
anaerobic and O2 -limited conditions
were not identified. Analysis of
N2 O evolved from NO3 − was
performed with gas
(JCM 6922), Streptomyces lavendulae
subsp. lavendulae (JCM 4664),
Streptomyces zelensis (JCM 5024) [42]
Streptomyces antibioticus (B-546) [46]
√
chromatography
N2 and N2 O in the gas phase were analysed by
gas chromatography. Observation: evolves N2
and some N2 O from NO3 − . Presence of
More recent literature not
available
√
denitrification together with
co-denitrification*
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Authors Journal compilation Biochemical Society Transactions (2011) Volume 39, part 1
Table S1 (Continued)
Species
Denitrification assessment
Current status
Streptomyces flavotricini (JCM 4371) [42]
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
Isolation of denitrifying
Gram-positive Streptomyces
strains from a soil denitrifying
[15 N]nitrite tracers). Observations: N2 O
evolution from NO3 − under anaerobic and
O2 -limited conditions and N2 O evolution from
NO2 − only under anaerobic conditions
Streptomyces thioluteus (JCM 4844) [42]
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observations: N2 O
evolution from both NO3 − and NO2 − under
anaerobic and O2 -limited conditions,
Micromonospora chalcea (JCM 3031),
Streptosporangium roseum (JCM 3005)
[42]
denitrification was accompanied by distinctive
cell growth. Purification of CuNir and azurin
N2 O in the gas phase was analysed by gas
chromatography and gas chromatography
Status
√
community [45], but the strains
were not identified. Analysis of
N2 O evolved from NO3 − was
performed with gas
chromatography
Isolation of denitrifying
Gram-positive Streptomyces
strains from a soil denitrifying
√
community [45], but the strains
were not identified. Analysis of
N2 O evolved from NO3 − was
performed with gas
chromatography
More recent literature not
available
√
spectrometry (with [15 N]nitrate and
[15 N]nitrite tracers). Observation: N2 O
evolution from both NO3 − and NO2 − under
anaerobic and O2 -limited conditions
(c) Non-spore-forming Gram-positive bacteria
Species
‘Corynebacterium nephridii’ [47]
Denitrification assessment
Denitrification by resting cells was measured
with Warburg respirometry and gas
measurements were performed by gas
chromatography. Only one strain is isolated,
N2 O is the end-product of denitrification
Corynebacterium sp. (12a) [41]
Denitrification was presumed positive if neither
NO2 − or NO3 − could be detected or showed
only traces in the supernatant after isolate
Current status
The ‘Corynebacterium nephridii’
strain was reported to be
Status
√
Gram-positive, but the strain is
actually Gram-negative [48].
Tiedje [49] mentions that the
strain probably is an
Alcaligenes sp.
More recent literature not
available
√
incubation. The final criteria for considering
an isolate a denitrifier were detection of nirS
Corynebacterium sp. (63k) [41]
or nirK by PCR followed by BLAST sequence
analysis. nirS (EU035284) gene was
sequenced
Denitrification was presumed positive if neither
NO2 − or NO3 − could be detected or showed
More recent literature not
available
√
only traces in the supernatant after isolate
incubation. The final criteria for considering
an isolate a denitrifier were detection of nirS
Gemella haemolysans [50]
or nirK by PCR followed by BLAST sequence
analysis. nirK (EU035280) gene sequenced
Only simple phenotypic testing† with
observation of gas formation was performed.
Observation: reduced low concentrations of
NO2 − , earlier studies reported
‘denitrification’
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Authors Journal compilation More recent literature not
available
−
Enzymology and Ecology of the Nitrogen Cycle
Table S1 (Continued)
Species
Denitrification assessment
Current status
Status
Jonesia denitrificans [51]
Technique for denitrification was not
mentioned in this species description.
Single isolate
Only observation of nitrates
reduced to nitrites [52]
−
Propionibacterium acidiproprionici [53]
Gas production from NO3 − was measured
by Warburg manometry. Denitrification
[reduction from NO3 − to gaseous
It was shown that
Propionibacterium
acidiproprionici strains did not
−
nitrogen (N2 O or N2 ) was
strain-dependent]
have respiratory denitrifying
ability, nor did they produce
N2 O at a rate typical for
respiratory denitrifiers, but they
did reduce NO2 − to N2 O in
nearly stochiometric amounts
Tsukamurella paurometabola [55]
NO2 − was utilized in some strains,
assessment of the denitrification
capacity was not performed
[49], maybe as a detoxifying
process [54]
More recent literature not
−
available
*Co-denitrification is the process in which a hybrid N2 or N2 O molecule is formed by combining two nitrogen atoms, one from NO3 − and one from
other nitrogen sources. The Actinomycetal hybrid N2 species appears to be formed from NO2 − (or NO) and not directly from NO3 − , since the
formation continues long after NO3 − is consumed.
†Simple phenotypic testing involves the observation of gas bubbles in Durham tubes and/or performance of Griess reduction tests or similar
techniques.
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(1996) Nitrite oxidation by heterotrophic bacteria under various
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Received 7 October 2010
doi:10.1042/BST0390254