Review
TRENDS in Microbiology
Vol.14 No.9
Microbial degradation of sulfur,
nitrogen and oxygen heterocycles
Ping Xu, Bo Yu, Fu Li Li, Xiao Feng Cai and Cui Qing Ma
State Key Laboratory of Microbial Technology, Shandong University, Jinan 250100, People’s Republic of China
Sulfur (S), nitrogen (N) and oxygen (O) heterocycles are
among the most potent environmental pollutants.
Microbial degradation of these pollutants is attracting
more and more attention because such bioprocesses are
environmentally friendly. The biotechnological potential
of these processes is being investigated, for example, to
achieve better sulfur removal by immobilized biocatalysts with magnetite nanoparticles or by solvent-tolerant bacteria, and to obtain valuable intermediates from
these heterocycles. Other recent advances have demonstrated the mechanisms of angular dioxygenation of
nitrogen heterocycles by microbes. However, these technologies are not yet available for large-scale applications
so future research must investigate proper modifications for industrial applications of these processes. This
review focuses on recent progress in understanding how
microbes degrade S, N and O heterocycles.
Hazardous heterocycles in the environment
Sulfur (S), nitrogen (N), and oxygen (O) heterocycles are
polycyclic aromatic compounds that contain one or more S,
N and/or O atoms in five- or six-membered rings (Figure 1).
S, N and O heterocycles and their degradation products
have been detected in groundwater, seawater, sediments,
soil and atmospheric samples. Their unusual toxicity and
mutagenicity call for great attention in studying such
chemicals [1]. S heterocycles, particularly dibenzothiophene (DBT) and its derivatives, can persist for up to three
years in the environment [2]. N heterocycles such as
carbazole and its derivatives are used in the production
of dyes, medicine and plastics [3] and, moreover, they
readily undergo radical chemical changes to generate
the more genotoxic hydroxynitrocarbazoles [4]. DBT and
carbazole are widely used as model compounds for the
study of biodegradation of polycyclic aromatic sulfurand nitrogen-containing hydrocarbons, respectively.
Dibenzofuran (DBF), an O heterocycle, has been used as
an insecticide and is formed from the photolysis of chlorinated biphenyl ethers [5]. DBF is a model for the biodegradation of chlorinated dibenzofurans and biaryl ethers
that are of great environmental concern. Owing to biological weathering processes, the environment is able to
handle these pollutants to a certain extent. Among such
processes, microbial degradation is a key method for
mineralization (the complete conversion of pollutants into
biomass or inorganic compounds) of these persistent toxic
Corresponding authors: Xu, P. ([email protected]);
Yu, B. ([email protected]).
Available online 24 July 2006.
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substances (PTSs) or persistent organic pollutants (POPs)
[6]. Therefore, it is necessary to investigate the fates of the
heterocycles that are metabolized by microorganisms.
Here, we review recent progress in understanding the
microbial metabolism of DBT, carbazole and DBF, and
provide a short introduction to the biotechnological potential of these transformations.
Mechanisms of heterocyclic biodegradation
S heterocycles: dibenzothiophene
DBT and its derivatives are the major sulfur-containing
aromatic compounds in fuels, accounting for up to 70% of
the sulfur content [7]. Many microorganisms such as
Rhodococcus [8], Mycobacterium [9] and Pseudomonas
species [10] can degrade DBT and the reactions can be
classified into three independent categories: sulfur oxidation, carbon–carbon cleavage and sulfur-specific cleavage.
The last category is the most extensively studied because a
sulfur atom is released from DBT, leaving the carbon
skeleton intact, which is useful in petroleum biodesulfurization [11]. Biotransformation of DBT by sulfur oxidation
is catalyzed by laccase from white rot fungi [12] and ring
dioxygenases from bacteria, which convert DBT into
dibenzothiophene sulfone and/or hydroxylated derivatives [13,14]. The carbon–carbon cleavage (Figure 2) by
which the carbon skeleton of DBT is broken following the
Kodama pathway has been reviewed previously [10]. This
enzymatic attack on the carbon atom is undesirable for a
process designed to remove organic sulfur compounds
selectively without oxidizing other aromatics in petroleum. In the sulfur-specific cleavage of DBT, 2-hydroxybiphenyl (2-HBP) is formed with the loss of sulfite. Until
recently, no DBT-desulfurizing microorganisms were
known to degrade 2-HBP further. Because there are many
publications on selective sulfur removal through the 4S
pathway, especially on the genetic and enzymatic mechanisms [10,11], here we focus only on the newly-reported
pathway: the extended 4S pathway in the sulfur-specific
cleavage category.
Li et al. [15] isolated a new thermophilic bacterium that
could initially desulfurize DBT to 2-HBP. The isolated
bacterium was identified as Mycobacterium goodii X7B
[15] and could further convert 2-HBP, the end product of
the 4S pathway, to 2-methoxybiphenyl (2-MBP). This
extended 4S pathway [9] is shown in Figure 3. The formation of the methoxylated product 2-MBP by Mycobacterium
sp. G3 was also detected. Although the substrate in the
methoxylation reaction was 2-HBP, there was no correlation between the expression of methoxylation activity and
0966-842X/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tim.2006.07.002
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Figure 1. Examples of sulfur, nitrogen and oxygen heterocycles that are found in environmental pollutants.
not yet clear. Recently, a similar strain was isolated that is
capable of degrading DBT – Microbacterium sp. ZD-M2 [19].
Besides 2-HBP and a small amount of 2-MBP, trace
amounts of biphenyl were also observed. As far as the
authors are aware, no other DBT-degrading strains capable
of converting 2-HBP to 2-MBP have been reported.
Although the mechanism of selective sulfur removal has
been studied for >15 years, none of these isolated strains
meet the industrial requirements of biodesulfurization,
which demand a high sulfur-removal rate, extensive sulfur
removal from heavy oils and decreased operation costs.
Therefore, a further detailed understanding of the metabolic mechanism is still expected and this will be the focus
of the majority of research.
Figure 2. Proposed Kodama pathway of DBT degradation through carbon–carbon
cleavage by Pseudomonas strains.
that of the desulfurization activity [16]. The alkylated
derivatives of DBT were also metabolized to their methoxy
forms by this pathway, and these results were consistent
with those obtained from Mycobacterium goodii X7B [9].
Many O-methyltransferases involved in methyl-transfer
reactions have also been reported [17,18] in which S-adenosyl-L-methionine functions as a methyl donor. For example, the conversion of abietic acid (a pesticide) to methyl
abietate is performed by the O-methyltransferase of Mycobacterium sp. MB3683 [18]. Okada et al. [16] expected that a
similar reaction system could be involved in the methoxylation process in Mycobacterium sp. G3 but the mechanism is
N heterocycles
Carbazole degradation by carbazole 1,9a-dioxygenase N
heterocycles such as carbazole and its derivatives are wellknown environmental pollutants in areas that have been
contaminated with wastes from coal gasification plants.
Most of the isolated species that degrade carbazole follow
a similar metabolic pathway in which the heterocycle
undergoes ring-cleavage to produce anthranilic acid as an
intermediate, which is then completely mineralized
[20–23]. In this pathway, carbazole is first degraded to
20 -aminobiphenyl-2,3-diol by carbazole 1,9a-dioxygenase
(CARDO) [24]. The novel catalytic mechanism of CARDO
has recently been clarified [25]. CARDO is a multicomponent enzyme and functional analysis revealed that the
CARDO of Pseudomonas resinovorans CA10 consists of
four parts: two terminal oxygenases (CarAa), a ferredoxin
(CarAc), and a ferredoxin reductase (CarAd) (Figure 4).
Figure 3. Proposed extended 4S pathway of DBT metabolism by Mycobacterium goodii X7B. DBT is converted to 2-hydroxybiphenyl by the traditional sulfur-specific
pathway in the initial steps. A new product, 2-methoxylbiphenyl, appeared in the M. goodii X7B desulfurizing process and was confirmed as the end product of this
pathway.
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Figure 4. The genetic arrangement and enzymatic mechanism of CARDO from Pseudomonas resinovorans CA10 [24]. CARDO is a multicomponent enzyme that catalyzes
the angular dioxygenation of carbazole to yield an unstable dihydroxylated intermediate, which is thought to be spontaneously converted to 20 -aminobiphenyl-2,3-diol.
Functional analysis revealed that CARDO consists of terminal oxygenase (CarAa), ferredoxin (CarAc) and ferredoxin reductase (CarAd) components (green arrows). Figure
reproduced, with permission, from Ref. [24].
Among the many reported aromatic compound
dioxygenases, CARDO is the only dioxygenase that can
catalyze cis-dihydroxylation, monooxygenation and angular dioxygenation on diverse aromatic compounds [13].
The catalytic component of CARDO, CarAa, has been
purified and crystallized and its 3D structure has been
determined [25]. CarAa from Janthinobacterium sp. J3
has a homotrimeric structure that governs the substrate
specificity of CARDO. The overall a3 trimeric structure of
the CarAa molecule approximately corresponds to the
partial a3 structure of other terminal oxygenase components of Rieske non-haem iron-oxygenase systems (ROSs)
that have the a3b3 configuration. The CarAa structure is the
first example of a terminal oxygenase component of a
ROS that has the a3 configuration. The shape of the
substrate-binding pocket of CarAa is markedly different
from those of other oxygenase components that are
involved in naphthalene and biphenyl degradation. The
results indicate that carbazole binds to the substratebinding pocket in a manner suitable for angular dioxygenation catalysis [25–27].
Although complete mineralization of carbazole is welcome in bioremediation, it is not suitable for the biotreatment of fossil fuels because the carbon value decreases
during the nitrogen removal process. However, a microorganism that can selectively cleave C–N bonds in quinoline and remove nitrogen from petroleum has been isolated
and characterized [28], and several Pseudomonas cultures
are well known for using carbazole as the sole nitrogen
source. Nevertheless, these bacteria cannot selectively
cleave both C–N bonds in carbazole while leaving the rest
of the molecule intact: the first step catalyzed by CARDO
converts carbazole to 20 -aminobiphenyl-2,3-diol, which
cleaves the first C–N bond, but there are no known deaminases that can metabolize 20 -aminobiphenyl-2,3-diol to
achieve cleavage of the final C–N bond. Recently, however,
a method for the selective cleavage of both C–N bonds of
carbazole was proposed. Genes that encode CARDO were
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combined with a genetically manipulated gene encoding an
amidase, which is suitable for selective cleavage of the C–N
bond in 20 -aminobiphenyl-2,3-diol. This approach formed
an operon, which encodes enzymes that catalyze the cleavage of both C–N bonds of carbazole [29]. This conversion of
carbazole could be a useful method for the selective
removal of recalcitrant organonitrogen compounds from
petroleum.
A novel attempt to combine two heteroatom-specific
degradation pathways in one biocatalyst could reduce
the operation costs that are associated with bioremediation
of S and N heterocycles. The well-known desulfurization of
DBT through the 4S pathway was combined with carbazole
conversion by Yu et al. [30], who introduced CARDO into a
DBT-degrader, Rhodococcus erythropolis XP. The recombinant could simultaneously degrade DBT and carbazole in
crude oil [30]. This study represents a new step towards the
development of biorefining processes. Future research
might enable the development of biocatalysts that can
simultaneously and selectively remove sulfur and nitrogen
from petroleum.
Carbazole degradation by other dioxygenases Carbazole
can also be metabolized by a hydroxylation reaction to form
monohydroxylated products. 3-Hydroxycarbazole is
detected as a major bioconversion product, whereas 1hydroxy- and 2-hydroxycarbazoles are observed as minor
products [31]. Bacterial dioxygenases often catalyze the
initial oxidation of aromatic hydrocarbons and related
heterocycles including carbazole. Naphthalene 1,2dioxygenase from Pseudomonas sp. NCIB 9816–4 and
biphenyl dioxygenase from Beijerinckia sp. B8/36 also
oxidize carbazole to 3-hydroxycarbazole but the toluene
dioxygenase from Pseudomonas putida F39/D does not
[32]. Biotransformation of carbazole to 3-hydroxycarbazole
is of great interest because hydroxylated carbazole
derivatives have strong antioxidant activity and are
value-added substances in the pharmaceutical industry,
Review
TRENDS in Microbiology
with a wide application in therapies for encephalopathy,
cardiopathy, hepatopathy and arteriosclerosis [31].
Degraded N heterocycles as pharmaceutical precursors
Nicotine is also an N-heterocyclic pollutant and is commonly
found in many solid, liquid and airborne wastes that are
generated during the tobacco manufacturing process.
The intermediates of nicotine degradation, 6-hydroxynicotine and 6-hydroxy-3-succinoyl-pyridine (HSP), are
useful precursors in the syntheses of insecticides and
pharmaceuticals [33]. An environmentally friendly
method of HSP production from nicotine in tobacco waste
has been developed [34] and this biotransformation is a good
example of how toxic wastes can be converted into valuable
compounds.
O heterocycles
Bacterial degradation of dibenzofuran Microbes that
degrade DBF are of increasing interest because of
their potential ability to co-metabolize highly toxic
polychlorinated
dibenzo-p-dioxins
(PCDDs)
and
polychlorinated dibenzofurans [35]. Here, only a brief
introduction to the DBF metabolic pathway is given [a
comprehensive review on the metabolism of dioxin-like
compounds (O heterocycles) by microorganisms is
available elsewhere [5]].
The initial steps in the biodegradation of DBF (Figure 5)
are categorized into three pathways: angular dioxygenation, lateral dioxygenation and lateral oxygenation. The
angular attack (Figure 5a) occurs at carbon atoms 4 and 4a
of DBF. Molecular oxygen is incorporated into the angular
position of DBF, which creates unstable hemiacetals that
break up spontaneously to yield 2,3,20 -trihydroxybiphenyl
(THBP). Subsequent ring cleavage of THBP is catalyzed by
extradiol dioxygenases to yield 2-hydroxy-6-(2-hydrophenyl)-6-oxo-2,4-hexadienoic acid, which is then hydrolyzed
to 3-(chroman-4-on-2-yl)-pyruvate and salicylic acid. Salicylic acid is then converted to catechol or gentisic acid.
These compounds are further degraded and channeled into
the tricarboxylic acid (TCA) cycle. Following this pathway,
which is similar to the carbazole-degradation process carried out by P. resinovorans CA10, DBF is completely
mineralized [3]. The initial angular dioxygenase, which
can react at the angular position adjacent to the oxygen
atom of DBF, is a key determinant of substrate range in the
degradation of aromatic compounds including dibenzo-pdioxins and other dibenzofurans [13]. Compared with other
initial dioxygenases such as naphthalene dioxygenases,
biphenyl dioxygenases and toluene dioxygenases, there
is still a lack of knowledge concerning angular dioxygenases [36].
By contrast, lateral dioxygenation, which is carried out
mainly by naphthalene- or biphenyl-utilizing bacteria,
occurs at the 1,2, the 2,3 and the 3,4 positions to produce
DBF-dihydrodiols (Figure 5b) [37,38]. Ring fission of 1,2dihydroxydibenzofuran results in the production of 2hydroxy-4-(30 -oxo-30 H-benzofuran-20 -ylidene)but-2-enoic
acid, which is degraded to salicylic acid. Salicylic acid is
then metabolized to catechol or gentisic acid followed by
incorporation into the TCA cycle, similar to the angular
dioxygenation pathway. The lateral dioxygenation
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401
pathway is also used in the co-metabolic degradation of
DBF by biphenyl-utilizing bacteria. There are only a few
reports of bacteria that transform DBF by both angular
and lateral dioxygenation [38–40].
Fungal degradation of dibenzofuran Although fungi
constitute the majority of microbial biomass in soil,
data on fungal catabolism of biaryl ether compounds are
limited and restricted to hydroxylation processes. A
fungus that can metabolize DBF (Figure 5c) was
identified as Trichosporon mucoides SBUG 801 [41]. The
accumulation of a high level of monohydroxylated DBF and
the formation of dihydroxylated derivatives from both
2-hydroxydibenzofuran and 3-hydroxydibenzofuran indicate the action of a monooxygenase during the initial
degradation steps. T. mucoides SBUG 801 degrades DBF
to 2,3-dihydroxydibenzofuran and subsequent ring cleavage
leads to the formation of 2-(1-carboxymethylidene)-2,3dihydrobenzo-[b]-furanylidene glycolic acid. Presumably,
cleavage of the dihydroxylated ring uses a mechanism
similar to that described for the degradation of biphenyl
ether by Trichosporon sp. SBUG 752. In both species, a third
hydroxyl group must be introduced into the dihydroxylated
intermediates before ortho cleavage of the aromatic
structure can take place [41].
Bioremediation continues to be an attractive option for
degradation of environmentally hazardous compounds.
The oxygen heterocyclic biodegradation studies described
here represent an important milestone in this field because
they demonstrate the possibility of aerobic biotransformation of POP substrates. A clearer understanding of the
biodegradation mechanism of wild-type strains or genetically modified bacteria will be beneficial to future bioremediation studies.
Environmental validity of heterocyclic biodegradation
Exploitation of the biodegradative activities of microorganisms to remove environmental pollutants and recalcitrant
xenobiotics is becoming more popular as an alternative to
physical and chemical methods because of the relatively
low cost and minimal impact on the environment. Many
researchers have focused their studies on the isolation and
identification of specific strains and some preliminary
applications, especially soil remediation, have been performed using bacteria [42]. The use of specific bacteria to
remove sulfur pollutants from petroleum will reduce the
amount of sulfur oxides released and, therefore, reduce
serious environmental pollution [11]. However, genetic
modifications to improve the sulfur removal efficiencies
of microorganisms are needed before a practical biorefining
process for the removal of sulfur compounds from petroleum can be developed. Genetically engineered microorganisms are required to remove the ‘heavier’ sulfur
compounds with more complex structures to an acceptable
level. Cultures with improved substrate ranges are also
needed to address the complicated mixture of chemicals
present in petroleum.
Unlike biodesulfurization, the biological removal of
nitrogen from petroleum (biodenitrogenation), has not
received much attention. So far, only a few reports have
been published and the reported nitrogen reduction is
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Figure 5. Three pathways of DBF degradation by microorganisms. The pathways are categorized according to initial steps in the biodegradation of DBF and are summarized
as angular dioxygenation, lateral dioxygenation and lateral oxygenation, respectively. (a) The angular attack occurs at the 4 and 4a carbon atoms of DBF. (b) Lateral
dioxygenation, mainly by naphthalene- or biphenyl-utilizing bacteria, occurs at the 1,2, the 2,3 and the 3,4 positions to produce DBF-dihydrodiols. (c) In lateral oxygenation,
monooxygenase catalysis during the initial degradation steps contributes to the accumulation of a high level of monohydroxylated DBF and the formation of
dihydroxylated derivatives from both 2-hydroxydibenzofuran and 3-hydroxydibenzofuran.
unsatisfactory [20,28]. This might be a result of the highly
complex nitrogen compounds and the diverse compound
structures present in petroleum, which cannot be degraded
by one type of nitrogen heterocycle-degrading strain alone.
Currently, no biocatalyst capable of selectively removing
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nitrogen is available, which also significantly limits the
development of biodenitrogenation processes.
Interestingly, the reported carbazole-degrader P. resinovorans CA10 can also detoxify poisonous oxygen compounds
and their chloro-derivatives such as PCDDs [35,43,44].
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TRENDS in Microbiology
Similar to the DBF-degrader Sphingomonas wittichii RW1,
carbazole-degraders have been used to mineralize these
PTSs or POPs, which cause serious environmental problems. Some initial experiments on soil bioremediation have
been carried out and good reductions were obtained [6].
Therefore, eradication of these persistent pollutants from
the environment has attracted much attention from academia, industry and governmental agencies. Bioremediation
by these heterocycle-degraders is likely to become a commercial prospect in the near future [45].
Solvent-tolerant bacteria for heterocyclic
biodegradation
At present, biotreatments of petroleum (especially biodesulfurization of petroleum-derived fractions such as diesel
oil and gasoline) face the problem of a high ratio of water to
oil in petroleum, which increases the reaction volume and
makes practical operations of biotreatments difficult. The
water-flooding techniques used to increase crude oil recovery in oilfields lead to a high ratio of water in crude oils,
which, by contrast, is more suitable for bacterial strain
survival and petroleum biodesulfurization. Therefore, it
would be more practical to incubate microorganisms in this
water–oil system before the water is removed [8,30].
Until now, there have been few reports concerning the
biodesulfurization of crude oil. R. erythropolis XP was
recently used to treat crude oil and gasoline samples
and a high level of sulfur removal was achieved [8,46].
However, the bacterium did not maintain a good desulfurization activity under high concentrations of oils.
By contrast, a biphasic system containing water-immiscible organic solvents has been exploited for biocatalysis
because it can integrate bioconversion and product recovery in a single reactor, overcome the problem of low
productivity in conventional media caused by poor substrate solubility and also shift chemical equilibrium to
enhance yields and selectivity [33,47]. However, many
organic solvents are highly toxic and can kill most
microorganisms even at low concentrations (e.g. 0.1% v/
v) [48], which makes the selection of biocompatible
solvents with the desired physicochemical properties a
difficult task. In addition, biotransformation is always
an energetically expensive multistep process. Cell integrity and viability are essential for this type of reaction [49].
It is reasonable to expect cells that maintain high
activity in a biphasic system to survive in the presence
of toxic organic solvents. Thus, microorganisms with
high tolerance to organic solvents are especially important
and useful in many biotechnological fields such as
biocatalysis [24,47]. Considering the difficulty of isolating
strains that have both solvent tolerance and the desired
catalytic activity from the environment, it might be
preferable to combine solvent-tolerance with unique
catalytic characteristics using genetic engineering.
Recently, Tao et al. [50] reported the introduction of
biodesulfurizing gene clusters into a solvent-tolerant bacterium. The resultant recombinant Pseudomonas putida
A4 could function even in the 50% p-xylene that was
present. This study is an important step towards exploring
novel biocatalysts for developing efficient bioprocesses in
biphasic reactions.
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Immobilization with magnetite nanoparticles
The use of immobilized microorganisms rather than free
cells in biotransformation can be advantageous to enhance
the stability of the biocatalyst and to facilitate its recovery
and re-use. These advantages have encouraged researchers to investigate the use of immobilized cells in bioconversion, biotransformation and biosynthesis processes
including oil biodesulfurization [15,51]. However, immobilization of cells using traditional entrapment methods has
major drawbacks. The mass-transfer problems of limited
diffusion and steric hindrance [47] reduce cell access to the
substrate and lead to a reduction in biotransformation
activity. As a result, immobilization by adsorption is currently gaining considerable importance because it reduces
(and in some cases eliminates) these mass-transfer problems associated with entrapment methods.
Techniques that immobilize microorganisms on nanoparticles have emerged as a novel aspect of the industrialization of cell immobilization because such particles have
a large specific surface area and high surface energy.
Recently, Shan et al. [52,53] reported the use of immobilized cells coated with magnetite (Fe3O4) nanoparticles in
biodesulfurization. The nanoparticles were surface-modified using ammonium oleate and then monodispersed in an
aqueous solution. Importantly, cells coated with magnetite
nanoparticles had the same biocatalytic activity as free
cells and could overcome the mass-transfer resistance of
traditional immobilization processes. Therefore, the nanoparticle-coated cells had greater desulfurizing activity
compared to traditional immobilization methods. This
attempt to develop efficient biocatalysts using immobilized
cells is a step towards improving biocatalysts for use in
many other fields such as biotransformation, biocatalysis
and biodegradation [54].
Concluding remarks and future perspectives
Although a more detailed understanding of all aspects of
the metabolic pathways is still needed, the understanding
of how microorganisms metabolize heterocycles is improving rapidly. Because only 0.1–1% of microorganisms can be
cultivated using current techniques, new techniques
including metagenomic methods have been developed to
explore novel genes and metabolic pathways for the biodegradation of recalcitrant and xenobiotic molecules [55].
Initial pilot-scale testing of microbial degradation of some
environmental pollutants by the cultures described earlier is under way, which should lead to lower costs for
biocatalyst preparation [56] and more efficient bacterial
degradation of hazardous compounds. A recent example is
the incorporation of a specialized membrane structure
termed a ‘superchannel’ into the dioxin-degrading
strain Sphingomonas wittichii RW1, which enabled the
direct incorporation of macromolecules into the recombinant cell and consequently increased the bioremediation
capability [57].
The emergence of new in vitro tools for mutation and
genetic rearrangement has enabled the limits of enzymatic
systems to be extended. Microorganisms with a wider
substrate range and higher substrate affinity in biphasic
reactions that contain toxic solvents or complex heterocycles could be engineered if the biocatalysts were to be
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TRENDS in Microbiology Vol.14 No.9
used for environmental remediation, petroleum treatment
or the production of bioderived compounds. These possibilities represent a future challenge for both microbiologists
and environmental engineers.
23
24
Acknowledgements
We gratefully acknowledge the support for our previous research from the
National Natural Science Foundation of China (grant numbers 20590368,
20377026, 30400008 and 20577031) and the Chinese National Programs
for High Technology Research and Development (grant number
2004AA649160).
25
26
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Elsevier celebrates two anniversaries with
a gift to university libraries in the developing world
In 1580, the Elzevir family began their printing and bookselling business in the Netherlands, publishing
works by scholars such as John Locke, Galileo Galilei and Hugo Grotius. On 4 March 1880, Jacobus
George Robbers founded the modern Elsevier company intending, just like the original Elzevir family, to
reproduce fine editions of literary classics for the edification of others who shared his passion, other
‘Elzevirians’. Robbers co-opted the Elzevir family printer’s mark, stamping the new Elsevier products
with a classic symbol of the symbiotic relationship between publisher and scholar. Elsevier has since
become a leader in the dissemination of scientific, technical and medical (STM) information, building a
reputation for excellence in publishing, new product innovation and commitment to its STM
communities.
In celebration of the House of Elzevir’s 425th anniversary and the 125th anniversary of the modern
Elsevier company, Elsevier donated books to ten university libraries in the developing world. Entitled
‘A Book in Your Name’, each of the 6700 Elsevier employees worldwide was invited to select one of
the chosen libraries to receive a book donated by Elsevier. The core gift collection contains the
company’s most important and widely used STM publications, including Gray’s Anatomy, Dorland’s
Illustrated Medical Dictionary, Essential Medical Physiology, Cecil Essentials of Medicine, Mosby’s
Medical, Nursing and Allied Health Dictionary, The Vaccine Book, Fundamentals of Neuroscience, and
Myles Textbook for Midwives.
The ten beneficiary libraries are located in Africa, South America and Asia. They include the Library of
the Sciences of the University of Sierra Leone; the library of the Muhimbili University College of Health
Sciences of the University of Dar es Salaam, Tanzania; the library of the College of Medicine of the
University of Malawi; and the University of Zambia; Universite du Mali; Universidade Eduardo
Mondlane, Mozambique; Makerere University, Uganda; Universidad San Francisco de Quito, Ecuador;
Universidad Francisco Marroquin, Guatemala; and the National Centre for Scientific and Technological
Information (NACESTI), Vietnam.
Through ’A Book in Your Name’, these libraries received books with a total retail value of
approximately one million US dollars.
For more information, visit www.elsevier.com
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