Formate dehydrogenase

FEMS MicrobiologyReviews87 (1990)377-382
Publishedby Elsevier
Formate dehydrogenase
James G. Ferry
Department of Anaerobic Microbiology, VirginiaPolytechnicInstitute and State University, 81acksbur~ U.S.A.
Key words: Aerobic microbiology; Anaerobic microbiology; Energy-conservingpathways; Biochemistry;
Molybdenum; Selenium; Molecular genetics; Molecular regulation
Formate is a substrate, or product, of diverse
reactions catalyzed by eukaryotic organisms,
eubacteria, and archaebacteria. A survey of
metabolic groups reveals that forraate is a common growth substrate, especially among the
anaerobic eubacteria and archaebacteria. Formate
also functions as an accessory reductant for the
utilization of more complex substrates, and an
intermediate in energy-conserving pathways. The
diversity of reactions involving formate dehydrogenases is apparent in the structures of electron
acceptors which include pyridine nucleotides, 5deazaflavin, quinones, and ferredoxin. This diversity of electron acceptors is reflected in the composition of formate dehydrogenase. Studies on
these enzymes have contributed to the biochemical
and genetic understanding of selenium,
molybdenum, tungsten, and iron in biology. The
regulation of formate dehydrogenase synthesis
serves as a model for understanding, general principles of regulation in anaerobic organisms.
A diversity of microorganisms produce or consume formate in a variety of metabolic pathways.
These include aerobic and anaerobic organisms
from among the eubacteria, archaebacteria and
eukaryotic yeasts. All contain the enzyme formate
dehydrogenase which catalyzes the reversible
two-electron oxidation of formate (HCOO- = CO2
+ H++ 2e-).
Among the aerobes, formate supports the
growth of several facultative, chemolithotrophic
eubacteria [1-3]. Methylotrophic organisms,
without the ribulose-5-phosphate cycle for carbon
assimilation, convert methanol to formate which is
further oxidized to carbon dioxide. Methylotrophic aerobes also utilize formate as a sole
source of energy. Recently, an electron transfer
system that transports electrons from formate to
nitrogenase was reported in extracts of the obligate methanotroph Methylosinus trichosporum [4].
In addition to formate, Pseudomonas oxalaticus
grows with oxalate as the .sole energy source, and
formate produced in this reaction is further
oxidized to carbon dioxide [5].
A greater diversity of anaerobic bacteria is able
to metabolize formate. The acid is produced during the fermentation of sugars catalyzed by pyrurate formate-lyase or by the reduction of carbon
dioxide [6]. Formate is also a product of the
Correspondence to: J.G. Ferry, Departmentof AnaerobicMicrobiology,VirginiaPolytechnicInstituteand State University.
Blacksbur8, VA 24061, U.S.A.
0168-6445/90/$03.50© 1990Federationof EuropeanMicrobiologicalSocieties
fermentation of aromatic compounds [7], L-( + )tartaric acid [8] and oxalate [9]. A recent report
suggests that the inward transport of divalent
oxalate is coupled to the outward movement of
the monovalent formate anion, and that this electrogenic antiport is the basis for energy coupling
in Oxalobacterformigenes [9]. Formate is an intermediate in nonsaccharolytic fermentations; it is
produced from formyltetrahydrofolate in the fermentation of purines and by reduction of carbon
dioxide during fermentation of hypoxanthine [10].
In the Wood pathway for the synthesis of acetate
[11], the methyl group is synthesized by reduction
of CO2 to formate followed by the formation of
formyltetrahydrofolate and reduction to methyltetrahydrofolate. The methyl group of methyltetrahydrofolate is transferred to a site on carbon
monoxide dehydrogenase where it condenses with
a carbonyl group (originating from CO2, CO or
the carboxyl group of pyruvate) and CoASH to
form acetyi-CoA. Many facultative and strictly
anaerobic bacteria obtain energy for growth by
electron transport phosphorylation coupled to the
oxidation of formate and reduction of exogenous
electron acceptors including nitrate and fumarate
[12]. Several anaerobic bacteria also contain a
formic hydrogenlyase system, but only a small
amount of energy is available from the conversion
of formate to H 2 plus CO2, and it is unlikely that
cells benefit. The sulfate-reducing bacteria are
strict anaerobes which obtain energy for growth
by the dis'~.nilatory reduction of sulfate to sulfide
[13]. The electron donors are diverse and include
H 2 and formate. In addition to sulfate, several
strictly anaerobic bacteria have been isolated that
reduce elemental sulfur, or oxides of sulfur, but
not sulfate. The strictly anaerobic methane-producing archaebacteria obtain energy for growth by
the cleavage of acetate or the reduction of carbon
dioxide [14]. The eight electrons required for the
reduction of carbon dioxide originate from H2 or
formate. The first one-carbon derivative in the
pathway is formylmethanofuran but free formate
is not an intermediate. The Methanobacterium formicicum formate dehydrogenase also participates
in a coenzyme F42o-mediatedformic hydrogenlyase
system [15]. Some homoacetogenic bacteria utilize
formate as a sole electron donor. Recently, it was
reported that Aiteromonas putrefaciens obtains energy for growth by the oxidation of formate and
reduction of Mn(IV) or Fe(III) [16]. In addition to
anaerobic respirations, organisms are described
that require H2 or formate as an accessory reductant for the fermentation of some organic substrates [17,18].
The conversion of complex organic matter to
methane in anaerobic freshwater habitats involves
microbial food chains comprised of interacting
metabolic groups (consortia) of organisms. The
fermentative bacteria degrade polymers to H 2,
formate, acetate, higher volatile fatty acids, and
other fermentation products. The H 2, formate,
and acetate are further degraded by the methaneproducing bacteria, terminal organisms of the consortia. The higher fatty acids, and other fermentation products, are cor~verted to methanogenic substrates by ~he acetog-~is. The acetogens rely on the
methanogens to lower the concentration of highly
reduced prt~duc~s, s~a'zethe oxidations are thermodynamically unfavo.rable. For historical reasons
this syntrophy is referred to as 'interspecies H 2
transfer" but recently a major involvement of formate in int~rspecies electron transfer was proposed [1~,19].
Table 1 lists the properties of formate dehydrogenases extensively purified from aerobic
organisms. All of these enzymes have a high K m
for formate, reduce NAD +, and are inhibited by
azide. The enzyme from P. oxalaticus is distinct
from all others in that it is a heterodimeric,
oxygen-sensitive, iron-sulfur, flavoprotein [20]; all
others are homodimeric with no known metals or
cofactors. The flavin dissociates from the P.
oxalaticus enzyme under reducing conditions
yielding an inactive deflavoprotein. Flavins are
generally required by dehydrogenases to transfer
electrons from one-electron centers to the obligate
two-electron accepting pyridine nucleotide. Thus,
the requirement for FMN implies that electrons
may be transferred from the iron-sulfur center to
Table 1
Properties of formate dehydrogenases extensivelypurified from
aerobic eubacteria and yeasts
molecular molecular
Referformate ences
a 2 (100000) 13.5
a 2 (46000)
a (48000)
a 2 (47000~
a 2 (46000)
a 2 (43000)
attain C-I
the flavin which d o n a t e s an electron pair to
N A D +.
Table 2 lists the properties of f o r m a t e dehydrogenuses purified from anaerobic archaebacteria
and eubacteria. All are extremely sensitive to
oxygen. Azide is a p o t e n t inhibitor, the only exception being the formate d e h y d r o g e n a s e f r o m
M e t h a n o c o c c u s vannieiii [26]. T h e enzymes c o n t a i n
a complex inventory of redox centers a n d reduce a
diversity of physiological electron acceptors, a
striking d e p a r t u r e f r o m the e n z y m e s o f aerobic
eubacteria a n d eukaryctes (Table 1). M a n y of the
purified enzymes contain a cofactor similar to the
6-substituted pterin ( m o l y b d o p t e r i n ) p r e s e n t in all
m o l y b d c e n z y m e s other t h a n nitrogenase [32]. T h e
cofactor f r o m the methanogenic a r c h a e b a c t e r i u m
M e t h a n o b a c t e r i u m f o r m i c i c u m is a 6-substituted
pterin, b u t apparentiy the structure of the side
chain is different f r o m the p r o p o s e d structure o f
the eukaryotic cofactor [33]. Interestingly, the side
Table 2
Properties of formate dehydrogenases extensively purified from anaerobic archaebacteria and eubacteria
Metals and
(mol/mol native)
1 Mo, 4.8-10.1 Fe
10-20 S
aj (85000)
BI (53000)
1 FAD, plcr~n
1 Mo, 2 Zn,
21-24 Fe, 25-29 S
Escherichia c
u4 (110000)
~4 (32000)
4 cytochrome b
4 Mo, 4 Se,
56 Fe. 52 S
a 2 (96000)
~z (76000)
2 W, 2 Se,
36 Fe. 50 S
Clostridium d
a I (76000)
/~l (34000)
pterin, 2 Mo,
24 Fe, 28 S
Vibrio c
a 2 (110000)
1 Mo,
19 Fe, 18 S
ND, not determined, b F420, 5-deazaflavin; ~ formate dehydrogenase coupled to nitrate reduction; d formate dehydrogenase
coupled to carbon dioxide reduction; e formate dehydrogenase coupled to fumarate reductase.
chain of the eubacterial molybdopterin
(bactopterin) from the carbon monoxide dehydrogenase of the aerobe Pseudomonas carboxydoflava
is structurally distinct from the eukaryotic cofactor [34]. The F420-reducing formate deh~drogenase
from M. formicicum is the only one reported to
contain flavin. Coenzyme F420 is an o01igate t~voelectron acceptor; thus, FAD is postulated to
shuttle electrons between one-electron centers and
1:42o [27]. In low-salt buffer FAD dissociates from
the enzyme under reducing conditions, or during
turnover, with loss of ability to reduce F420. The
presence of flavins has not been reported for
either the F420- or NADP-reducing enzymes from
M. vannielii or CIostridium thermoaceticum.
Selenium is a c o , n o n , but not essential, componew. of formate dehydrogenases from anaerobic
organism.% The metal is present in a selenocysteine residue of the largest subunit of the formic
hydrogeniyase-linked formate dehydrogenase from
E. coli ~35]. Comparison of the deduced amino
acid sequences of the large subunits from the
selenium-dependent formate dehydrogenase from
E. coli and the selenium-independent enzyme from
M. formicicum reveals high overall identity [36,37].
The methanogen enzyme shares striking identity
with the E. coli enzyme in the regions flanking the
selenocysteine; interestingly, the methanogen enzyme contains cysteine in the position corresponding to selenocysteine in the E. coli enzyme. The
conservation of this sequence in both enzymes
implies that it supports a common function.
Relatively little is known of the genetics of
formate dehydrogenases from aerobic organisms.
Conversely, the regulation of anaerobic metabolism (including the synthesis of the formic hydrogenlyase-linked formate dehydrogenase-H) has
been extensively studied in E. coll. An active fnr
gene product is required for expression of
anaerobically inducible genes which encode
pyruvate formate-lyase and enzymes catalyzing the
formate-dependent reduction of fumarate, trimethylamine-N-oxide, or nitrate [38]. Anoxic
growth in the presence of these electron aeceptors
repre.~ses synthesis of the formic hydrogenlyase
system in order to direct electron flow from formate t~.~rds reduction of the electron acceptors.
During fermentative metabolism (in the absence
of exogenous electron acceptors), formate is required for expression of the formic hydrogenlyase
system. A mutant, defective in pyruvate formatelyase, requires exogenously supplied formate
for transcription of at least two genes involved in
the synthesis of formic hydrogenlyase [39]: the
fdhF gene encoding the M r = 80000 subunit of
formate dehydrogenase-H, and hyd-17 required
for hydrogenase-3 expression. Anaerobic expression and induction of formate dehydrogenase-H
by formate depends on a region of 185 nucleotidcs
upstream of the translational start of the fdhF
gene [39,40]. The fnr gene product does not interact with the regulatory sequence; instead, a sigma
factor is involved in the regulation of transcription. Recently, mutations in trans were reported
which affect the anaerobic expression of the fdhF
gene [41]. Molybdate is required for transcription
of fdhF [40]; however, mutations blocking the
synthesis of functional molybdopterin cofactor
have no influence on the transcription of fdhF
and hyd-17, indicating that the cofactor is not
involved in regulation [39,42]. Recently, it was
reported that the hark gene product is involved in
nitrate repression of fdhF and hyd-17 [43].
Incorporation of selenocysteine into the formate dehydrogenase-H of E. coli is through
cotranslational insertion directed by an in-frame
UGA stop codon [37]. Translation of the UGA
codon requires a functional pathway for incorporation of selenocysteine. Four genes have been
identified: the selA and selB genes with unknown
function, the seIC gene coding for the functional
tRNA which inserts selenocysteine into protein
[44], and seiD which is involved in selenium incorporation into protein or tRNA.
The genetics of formate dehydrogenase-N (linked to the reduction of nitrate) of E. coli have
been studied in parallel with nitrate reductase.
Genes involved in the synthesis of active molybdopterin for both enzymes are designated chlA,
chlB, chlD, chiE. Mutations in the chl genes also
effect the synthesis of an active formate dehydrogenase-N and formate dehydrogenase-H [45-47].
T h e chIB gene p r o d u c t ( F A factor) facilitates ass e m b l y of active nitrate reductase which implies a
similar function for the formate dehydrogenase,
possibly m o l y b d o p t e r i n insertion into apoenzymes. The chlD gene is involved in m o l y b d e n u m
processing w h e n cells are g r o w n with low concentrations o f m o l y b d a t e [48]. F o r m a t e dehydrogenase-N is not synthesized in a chlD b a c k g r o u n d
unless the m u t a n t cells are s u p p l e m e n t e d with
high concentrations of m o l y b d a t e to circumvent
the chID requirement [46]. M u t a n t s of E. coli are
described which are deficient in formate dehydrogenase-N b u t not f o r m a t e d e h y d r o g e n a s e - H [49].
T h e genes encoding the two s u b u n i t s of the
f o r m a t e dehydrogenase f r o m M. formlcicum have
been cloned and sequenced [36]. Analysis of sequences u p s t r e a m o f the transcriptional start site
reveal a potential archaebacteria p r o m o t e r , and
additional sequences with considerable identity to
sequences u p s t r e a m of the E. coii f d h F gene [50].
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