Pyrimidine Base Catabolism in Species of Pseudomonas and Burkholderia
Thomas P. West
Three distinct pathways to degrade pyrimidine bases in bacteria have been identified. The prevalent pathway of pyrimidine catabolism in species of Pseudomonas and Burkholderia is the reductive pathway. The reductive pathway consists of three enzymatic steps where uracil or thymine is degraded to β-alanine or β-aminoisobutyric acid, respectively. The enzymes dihydropyrimidine dehydrogenase, dihydropyrimidinase and β-ureidopropionase have been detected in a number of species of Pseudomonas and Burkholderia. The bacterial cell from these species were grown on pyrimidine bases as sole nitrogen sources and assayed for pyrimidine reductive catabolic enzyme activities using previously described assayed procedures. The three enzyme activities have been found to increase several fold depending upon the source of nitrogen and carbon used to grow the microorganisms. In species of Pseudomonas as well as Burkholderia cepacia, it was observed that pyrimidine bases induced the synthesis of the pyrimidine reductive pathway enzymes. The induction of the reductive pathway enzymes as well as other salvage enzymes in B. cepacia by 5-methylcytosine may indicate that pyrimidine catabolism in species of Pseudomonas and Burkholderia involves two additional enzymes. This possibility needs to be investigated to better understand whether pyrimidine catabolism is these microorganisms is more complex than originally thought. Overall, species of Pseudomonas and Burkholderia utilize the reductive pathway to provide a source of nitrogen from the catabolism of pyrimidine bases under nitrogen-limiting growth conditions.
April 23, 2010; Accepted: May 30, 2010;
Published: September 30, 2010
The catabolism of the pyrimidine bases uracil and thymine has been shown to
provide a source of nitrogen in prokaryotes. It has been established that three
different types of pyrimidine catabolic pathways exist in prokaryotes (Vogels
and van der Drift, 1976). One pathway involves the oxidative catabolism
of uracil and thymine to urea and malonic acid by the enzymes uracil/thymine
dehydrogenase, barbiturase and ureidomalonase (Vogels and
van der Drift, 1976; Soong et al., 2001,
2002). Strains of Nocardia, Mycobacterium
and Enterobacter aerogenes and Rhodococcus erythropolis degrade
pyrimidine bases using the oxidative pathway (Hayaishi and
Kornberg, 1952; Lara, 1952; Patel
and West, 1987; Soong et al., 2001,
2002). A second pathway of pyrimidine catabolism has been recently identified
in Escherichia coli K-12 (Loh et al., 2006).
It has been found that this pathway degrades uracil and thymine to 3-hydroxypropionic
acid and 2-methyl-3-hydroxypropionic acid, respectively and operates at room
temperature but not at 37°C (Loh et al., 2006).
The third pathway of pyrimidine catabolism is called the reductive pathway and
it appears to be more prevalent in prokaryotes than the other types of pyrimidine
catabolic pathways (Vogels and van der Drift, 1976).
||The pyrimidine base reductive catabolic pathway enzymes include
(1) dihydropyrimidine dehydrogenase, (2) dihydropyrimidinase and (3) β-ureidopropionase
The reductive pathway involves three enzymatic steps (Fig. 1).
The initial step is catalysed by the enzyme dihydropyrimidine dehydrogenase
(EC 22.214.171.124) that converts uracil and thymine to dihydrouracil and dihydrothymine,
respectively (Fig. 1). The second pathway step is catalyzed
by the enzyme dihydropyrimidinase (EC 126.96.36.199), which converts dihydrouracil
and dihydrothymine, respectively, to N-carbamoyl-β-alanine and N-carbamoyl-β-aminoisobutyric
acid (Fig. 1). This enzyme usually also has the ability to
hydrolyze hydantoins and this could prove vital in the development of large-scale
bioreactor systems for the inexpensive production of β-amino acids and
D-amino acids (Morin et al., 1986; Chevalier
et al., 1989; Sharma and Vohra, 1999;
Zhang et al., 2010). The final step of the reductive pathway is catalysed
by the enzyme β-ureidopropionase (EC 188.8.131.52). This enzyme produces β-alanine
or β-aminoisobutyric acid from their respective N-carbamoyl derivatives
(Fig. 1). The reductive pathway operates in a number of prokaryotes
including Clostridium uracilicum (Campbell, 1957),
Acidovorax facilis (Kramer and Kaltwasser, 1969),
Salmonella typhimurium (West et al., 1985)
and Escherichia coli B (West, 1998). A number
of pseudomonad species, including Pseudomonas aeruginosa (Potter
et al., 1982; Kim and West, 1991), Pseudomonas
chlororaphis (West, 1991a), Pseudomonas stutzeri
(Xu and West, 1992), Pseudomonas fluorescens
(Santiago and West, 1999), Pseudomonas putida
(West, 2001), Pseudomonas lemonnieri (Burnette
et al., 2006) and Pseudomonas syringae (Gant
et al., 2007), have been shown to utilize the reductive pathway to
degrade pyrimidine bases. The related species Burkholderia cepacia also
degraded pyrimidine bases using the reductive pathway (West,
1997). Many of the fluorescent pseudomonads are recognized to be clinically
significant in humans. The role of the fluorescent pseudomonads as opportunistic
pathogens during the treatment of human cancer with such chemotherapeutic agents
as 5-fluorouracil has been noted (Moody et al., 1972).
The species P. aeruginosa and B. cepacia are known human pathogens
afflicting individuals with cystic fibrosis as well as human burn patients (Eberl
and Tummler, 2004). Another pseudomonad of importance is P. syringae,
which is a known plant pathogen (Salch and Shaw, 1988).
Considering the significance of the pseudomonad species and B. cepacia as
pathogens, catabolism of pyrimidine bases was studied in these strains to better
understand how these microbes survived under nitrogen-limiting conditions and
to identify possible mechanisms of microbiological control.
Enzyme function: Dihydropyrimidine dehydrogenase reduces the pyrimidine
bases uracil and thymine using a nicotinamide cofactor. Maximal enzyme activity
is observed with either NADH or NADPH as a nicotinamide cofactor.
|| Nicotinamide cofactor specificity of dihydropyrimidine dehydrogenase
from pseudomonads and Burkholderia cepacia
|+: Presence; -: Absence
A possible explanation for the pseudomonad dehydrogenase activity being active
using either cofactor is likely related to the presence of pyridine nucleotide
transhydrogenase (EC 184.108.40.206) in pseudomonad cells (Kaplan,
1955). This enzyme catalyzes a reaction involving the reduction of either
NAD+ or NADP+ to synthesize NADH or NADPH (San
Pietro et al., 1955; French et al., 1997).
NADH is the preferred nicotinamide cofactor for the P. aeruginosa, P.
chlororaphis, P. putida, P. stutzeri or P. syringae
dihydropyrimidine dehydrogenase (Table 1). NADPH serves as
the preferred nicotinamide cofactor for dihydropyrimidine dehydrogenase in P.
fluorescens, P. lemonnieri and B. cepacia (Table
1). In P. pseudoalcaligenes ATCC 17740, the preferred nicotinamide
cofactor for the dehydrogenase present in cells grown at 30°C with aeration
in an orbital shaker (200 revolutions min-1) on 0.2% uracil as a
nitrogen source and 0.4% succinate as a carbon source was found to be NADH (T.P.
West, unpublished results). The cells were processed and assayed as previously
described (West, 1991b). Dehydrogenase specific activity
was 2.32 nmol dihydrouracil formed/min/mg protein (within 10% error) using NADH
as a cofactor compared to 0.10 nmol dihydrouracil formed/min/mg protein (within
10% error) using NADPH as a cofactor (T.P. West, unpublished results). Similarly,
NADH was the preferred nicotinamide cofactor for the dehydrogenase present in
cells grown at 30°C with aeration in an orbital shaker (200 revolutions
min-1) on 0.2% thymine as a nitrogen source and 0.4% succinate as
a carbon source. Dehydrogenase specific activity was 0.97 nmol dihydrouracil
formed/min/mg protein (within 10% error) using NADH as a cofactor compared to
0.36 nmol dihydrouracil formed/min/mg protein (within 10% error) using NADPH
as a cofactor (T.P. West, unublished results).
Effect of growth conditions: Dihydropyrimidine dehydrogenase activity
in species of Pseudomonas and Burkholderia is influenced by the
source of nitrogen and carbon. Maximum dehydrogenase activity was observed in
P. aeruginosa, P. chlororaphis, P. lemonnieri or P.
syringae when the cells were grown on uracil as a nitrogen source and glucose
as a carbon source compared to cells grown in a glucose minimal medium containing
ammonium sulfate as the nitrogen source (Table 2). In P.
pseudoalcaligenes or P. putida, dehydrogenase activity was highest
when the cells were grown on uracil as a nitrogen source and succinate as a
carbon source relative to cells grown in a succinate minimal medium containing
ammonium sulfate as the nitrogen source (Table 2). When P.
fluorescens cells were grown on dihydrouracil as a nitrogen source and succinate
as a carbon source, maximum dehydrogenase activity was observed compared to
cells grown on ammonium sulfate and succinate. Growth on thymine as a nitrogen
source and succinate as a carbon source produced the largest increase in dehydrogenase
activity in P. stutzeri (Table 2). In B. cepacia,
glucose-grown cells produced the highest dehydrogenase activity using 5-methylcytosine
as a nitrogen source (Table 2).
||Growth conditions found to produce maximum dihydropyrimidine
dehydrogenase activity in species of Pseudomonas species and Burkholderia
Clearly, the source of nitrogen greatly affected the level of dehydrogenase
activity in species of Pseudomonas and Burkholderia.
Enzyme function: Relative to the species of Pseudomonas and Burkholderia,
only the P. stutzeri dihydropyrimidinase has been characterized from
cells growth on dihydrothymine as a nitrogen source and succinate as a carbon
source (Xu and West, 1994). The partially purified enzyme
has a molecular weight of 115,000 daltons (Xu and West,
1994). The P. stutzeri enzyme was found to utilize dihydrouracil,
dihydrothymine and hydantoin as substrates (Xu and West,
1994). The optimal temperature for enzyme activity was 45°C and it was
active between pH 7.5-9.0 (Xu and West, 1994). The P.
stutzeri enzyme was stimulated by magnesium ions and inhibited by zinc or
copper ions (Xu and West, 1994). Although, the dihydropyrimidinase
from P. stutzeri could utilize hydantoin as a substrate, it was more
specific for the dihydropyrimidine bases as substrates (Xu
and West, 1994). Therefore, it appeared that a dihydropyrimidinase activity
was present in P. stutzeri although the presence of a D-hydantoinase
activity was not investigated.
Effect of growth conditions: Growth on either pyrimidine or dihydropyrimidine
bases increased the levels of dihydropyrimidinase activity in the species of
Pseudomonas and Burkholderia. Growth of B. cepacia cells
on the nitrogen source 5-methylcytosine and the carbon source glucose resulted
in the highest observed dihydropyrimidinase activity (Table 3).
In P. aeruginosa, growth on uracil as a nitrogen source and glucose as
a carbon source produced the highest dihydropyrimidinase activity (Table
3). Succinate-grown cells of P. fluorescens or P. putida exhibited
the maximum dihydropyrimidinase activity when thymine served as the nitrogen
source (Table 3). In P. pseudoalcaligenes, P. stutzeri
or P. syringae, dihydropyrimidinase activity was increased to the highest
observed level of activity following cell growth on dihydrothymine as a nitrogen
source and succinate as the carbon source (Table 3). Glucose-grown
cells of P. lemonnieri produced the highest dihydropyrimidinase activity
when dihydrouracil served as the nitrogen source (Table 3).
With respect to dihydropyrimidinase activity in P. chlororaphis ATCC
17414, growth of the cells on the nitrogen source dihydrothymine and carbon
source glucose resulted in over a 100-fold increase in its activity (Table
3). Using two types of colorimetric assays, it has also been determined
that a hydantoin-hydrolyzing activity exists in P. chlororaphis ATCC
17414 in addition to dihydropyrimidinase. When P. chlororaphis ATCC
17414 cells were grown with aeration in an orbital shaker (200 revolutions min-1)
at 30°C in a medium containing 0.2% hydantoin as a nitrogen source and 0.4%
glucose as a carbon source and the cells were processed and assayed as previously
described (West, 1991a), it was possible to detect hydantoinase
activity in this strain (T.P. West, unpublished results).
|| Growth conditions shown to produce maximum dihydropyrimidinase
activity in Pseudomonas species and Burkholderia cepacia
A comparison of dihydropyrimidinase and hydantoinase activities was made in
the hydantoin-grown cells at 45°C where 5 mM substrate (dihydrouracil or
hydantoin) was included in the reaction mix. Under these conditions, the specific
activity of dihydropyrimidinase was <0.06±0.01 nmol/min/mg protein
(standard deviation) while the hydantoinase specific activity was 16.68±2.98
nmol/min/mg protein (±standard deviation). Both of these enzyme activities
were also assayed in the extracts derived from hydantoin-grown cells at a lower
substrate concentration (1 mM) and at a lower assay temperature (30°C).
It was determined that the dihydropyrimidinase specific activity was 6.63±0.69
nmol/min/mg protein (±standard deviation) while the hydantoinase specific
activity was 0.53±0.07 nmol/min/mg protein (T.P. West, unpublished results).
The different activities observed would seem to indicate that the enzymes dihydropyrimidinase
and hydantoinase exist independent of one another in P. chlororaphis
ATCC 17414 cells. Dihydropyrimidinase activity has also been detected in P.
putida (Takahashi et al., 1978; Chevalier
et al., 1989; West, 2001). In P. putida
strain RU-KM3S, the inactivation of the gene encoding dihydropyrimidinase resulted
in the loss of hydantoinase activity suggesting that dihydropyrimidinase was
responsible for the observed hydantoinase activity (Matcher
et al., 2004). It does not appear that dihydropyrimidinase is solely
responsible for hydantoin hydrolysis in Pseudomonas species because a
DNA probe from P. putida to detect D-hydantoin-producing microorganisms
found that they contained a gene for a D-hydantoinase (LaPointe
et al., 1995). The presence of both a dihydropyrimidinase activity
and a hydantoinase activity has been confirmed in P. fluorescens (Morin
et al., 1986) similar to what was observed in P. chlororaphis
cells. It has been found that resting cells of B. cepacia produced
a D-hydantoinase from a hydantoin when corn steep liquor served as the nitrogen
source (Jiang et al., 2007). Overall, previous
work indicates that growth of pseudomonads or B. cepacia on pyrimidine
or dihydropyrimidine bases as nitrogen sources resulted in an elevation of dihydropyrimidinase
activity that likely exists independently of the hydantoin-hydrolyzing activity.
Enzyme function: A prior study has purified β-ureidopropionase
to homogeneity from P. putida IFO12996 (Ogawa and
Shimizu, 1994). It was found to have a molecular weight of 90,000 daltons
and require the presence of a divalent metal ion for activity (Ogawa
and Shimizu, 1994). The enzyme has a broad substrate specificity for N-carbamoyl-α-amino
acids and the hydrolysis of the N-carbamoyl-α-amino acids was noted to
be L-enantiomer specific (Ogawa and Shimizu, 1994).
|| Growth conditions shown to produce maximum β-ureidopropionase
in Pseudomonas species and Burkholderia cepacia
|β-AIA, β-aminoisobutyric acid.
The properties of the P. putida β-ureidopropionase were shown to
differ from those previously observed in an anaerobic bacterium (Campbell,
Effect of growth conditio ns: Growth of the species of Pseudomonas
and Burkholderia on pyrimidine bases, dihydrouracil, β-alanine and
β-aminoisobutyric acid as nitrogen sources increased their cellular levels
of β-ureidopropionase activity compared to growth on ammonium sulfate as
a nitrogen source. When glucose-grown cells of P. aeruginosa or P.
fluorescens utilized uracil as a nitrogen source, β-ureidopropionase
was elevated to its highest activity level (Table 4). Similarly,
glucose-grown cells of B. cepacia exhibited their highest enzyme activity
when thymine served as the nitrogen source (Table 4). The
dihydropyrimidine base uracil produced the greatest elevation of β-ureidopropionase
activity in glucose-grown cells of P. stutzeri or P. syringae
when it served as a nitrogen source (Table 4). In P. lemonnieri,
the product of the β-ureidopropionase reaction, namely β-alanine,
increased its enzyme activity when succinate-grown cells utilized β-alanine
as a source of nitrogen (Table 4). The other product of the
β-ureidopropionase reaction, namely β-aminoisobutyric acid, produced
the highest enzyme activity in glucose-grown P. putida cells that used
β-aminoisobutyric acid as the source of nitrogen (Table 4).
Although, dihydropyrimidine dehydrogenase and dihydropyrimidinase activities
in the pseudomonads and B. cepacia responded to growth on pyrimidines
and dihydropyrimidines as nitrogen sources, it appeared that only β-ureidopropionase
activity in pseudomonads was affected by growth on β-alanine or β-aminoisobutyric
acid as a nitrogen source (Table 4).
REGULATION AT THE LEVEL OF ENZYME SYNTHESIS
With the pyrimidine catabolic enzyme activities of the species of Pseudomonas
and Burkholderia being affected by growth on pyrimidine bases and their
catabolic products as nitrogen source, it appeared likely that the catabolic
pathway was regulated at the level of enzyme synthesis. In pseudomonads, it
has been found that many catabolic pathways of aromatic compounds are subject
to regulation by induction of enzyme synthesis by substrates (Ornston
and Parke, 1977). Uracil has been found to induce the synthesis of the reductive
pathway enzymes in P. aeruginosa and P. fluorescens when glucose
served as the carbon source while it was also noted to induce enzyme synthesis
in P. putida when succinate served as the carbon source (Table
5). In P. stutzeri, thymine was the inducer of reductive pathway
enzyme synthesis when succinate served as the carbon source (Table
5). The inducer of reductive pathway enzyme synthesis in B. cepacia
was 5-methylcytosine when glucose was the carbon source (Table
5). Pyrimidine bases were shown to control pyrimidine reductive pathway
enzyme synthesis in all prior studies examining species of Pseudomonas
and Burkholderia (Kim and West, 1991; Xu
and West, 1992; West, 1997; Santiago
and West, 1999; West, 2001).
|| Growth conditions found to induce pyrimidine catabolic enzyme
activities in pseudomonads and Burkholderia cepacia
From the prior investigations, it is clear that pyrimidine base catabolism
is subject to control at the level of enzyme transcription.
It can be concluded that species of Pseudomonas and Burkholderia
actively degrade uracil and thymine using the reductive pathway. It is also
clear that the levels of the reductive pathway enzyme activities in these species
depend upon the source of nitrogen provided in the growth medium. Further, the
three enzyme activities in species of Pseudomonas and Burkholderia
are inducible when pyrimidine bases serve as the nitrogen source. It remains
to be investigated in these species whether the pyrimidine reductive catabolic
pathway consists of only three enzymes or whether it is a pathway consisting
of five enzymes. In B. cepacia, 5-methylcytosine has been found to induce
the pyrimidine catabolic pathway enzymes. It has been previously shown that
the enzyme cytosine deaminase purified from Pseudomonas aureofaciens
was capable of deaminating cytosine or 5-methylcytosine to uracil or thymine,
respectively (Sakai et al., 1975) and the enzyme
is an important pyrimidine salvage enzyme in pseudomonads (Sakai
et al., 1976; Beck and ODonovan, 2008).
Cytosine deaminase, which provides the substrates to the dihydropyrimidine dehydrogenase
reaction, was induced by 5-methylcytosine in B. cepacia (West,
2000). Similarly, the enzyme β-alanine-pyruvate transaminase that degrades
the products of the β-ureidopropionase reaction is induced by 5-methylcytosine
in B. cepacia (West, 2000). The ability of 5-methylcytosine
to induce the enzymes cytosine deaminase, dihydropyrimidine dehydrogenase, dihydropyrimidinase,
β-ureidopropionase and β-alanine-pyruvate transaminase in pseudomonads
needs to be more fully explored. It may be that the five enzymes work in unison
to degrade the pyrimidine bases that result from nucleic acid catabolism to
provide a source of nitrogen for the cells. It also need to be clarified whether
species of Pseudomonas and Burkholderia synthesize both dihydropyrimidinase
and hydantoinase activities. It may be that the dihydropyrimidinase and hydantoinase
are stereospecific to produce D- or L-enantiomers (Syldatk
et al., 1999). Each enzyme activity may only be synthesized under
specific growth conditions for species of Pseudomonas and Burkholderia.
Further, investigations need to determine more fully the role of each enzyme
in bacterial metabolism.
This research was supported by the South Dakota Agricultural Experiment Station. The technical assistance of Beth Nemmers during the pyrimidine catabolism studies was greatly appreciated.
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