C3
Bacterial degradation of lignin
RAFAEL VICUNA
Unidad de Microbiologia y GenOtica Molecular,
Pontificia Universidad CatOlica de Chile,
Casilla I14-D. Santiago, Chile
Summary. During the year 1983, there was a breakthrough in
the field of lignin biodegradation when fungal ligninases and
their hydrogen peroxide requirement were described. A
comparable progression has not yet occurred with lignino-
lytic bacteria, although it is expected to take place in the
near future once depolymerizing enzymes are isolated. Sev-
eral bacterial strains have been found to mineralize aerobi-
cally [14C-lignin]lignocellulose as well as 14C-labelled syn-
thetic lignins, even though the most efficient are still far
from reaching the rates exhibited by ligninolytic fungi. Acti-
nomycetes follow a characteristic pattern of lignocellulose
decomposition, with the release of lignin-rich, water-soluble
fragments that are slowly metabolized thereafter. Research
is being carried out to find the key enzymes involved in both
lignin solubilization and mineralization by bacteria and un-
cover their mechanism of action. The ability of bacteria to
grow on low-molecular-weight lignin oligomers as the sole
source of carbon and energy indicates that bacteria produce
enzymes catalysing cleavage of intermonomeric linkages.
Various strains metabolize cyclic lignans, biphenyl struc-
tures, and other "dimeric" compounds, including those that
possess the arylglycerol -fl-aryl ether (fl-O-4) linkage. Clea-
vage of the latter apparently is reductive, fl-O-4 dimers be-
ing metabolized by some bacteria through Cc~-Cfl cleavage.
In contrast, no one has isolated a bacterium capable of
decomposing a dimeric structure of the 1,2-diarylpropane-
1,3-diol (fl-1) type, although strains metabolizing 1,2-diaryl-
ethane compounds have been found. In the absence of oxy-
gen, only low-molecular-weight oligomers or chemically
modified lignins are significantly degraded. The contribution
of bacteria to the complete biodegradation of lignin in natu-
ral environments where fungi are also present is not known.
However, bacteria seem to play a leading role in decom-
posing lignin in aquatic ecosystems.
Keywords: Lignin;lignocellulose; lignin-related compounds;biode-
gradation; ligninolytic bacteria
Introduction
Bacteria are known to display an ample metabolic ver-
satility towards aromatic substrates. This characteris-
tic applies for naturally occurring compounds, as well
as for those of xenobiotic origin. (i.e., polycyclic aro-
matic hydrocarbons, halogenated biocides, azo dyes,
etc.). The high rate of genetic adaptation exhibited by
these microorganisms has contributed to enable them
to develop this versatility through evolution. 1,2
Lignin is by far the most abundant aromatic sub-
stance present in the biosphere. It is a polymer com-
posed of phenylpropanoid units linked through a vari-
ety of nonhydrolysable C--C and C--O--C bonds. 3
Bacteria of several genera, including Pseudomonas,
Alcaligenes, Arthrobacter, Nocardia, and Strepto-
myces, readily degrade the single-ring aromatic com-
pounds that build up the lignin macromolecule. 4-s
However, the extent to which bacteria are able to
bring about the decay of the lignin polymer itself has
not been properly assessed. In part this is because
lignin biodegradation studies have concentrated on
filamentous fungi. For example, in recent meetings in
this field,9'1° presentations on ligninolytic fungi out-
numbered those on bacteria by a factor of seven. This
is understandable, since some species of the former
can efficiently mineralize lignin. In contrast, informa-
tion available to date indicates that lignin is fairly re-
calcitrant to bacterial attack, at least under laboratory
conditions. For this reason, some authors believe that
bacteria play a secondary role in lignin biodegradation
in natural environments.~l-14
Lignin breakdown involves multiple biochemical
reactions that have to take place more or less simulta-
neously: cleavage of intermonomeric linkages, de-
methylations, hydroxylations, side chain modifica-
tions, and aromatic ring fission followed by
dissimilation of the aliphatic metabolites produced. In-
solubility of lignin and its lack of stereoregularity con-
tribute to making it a substrate that is difficult for the
microflora to degrade. Fungi overcome these con-
straints by virtue of a family of extracellular iso-
enzymes collectively called "ligninases, ''15-19 which
are peroxidases that act through a mechanism involv-
ing free radical formationfl ° Bacterial counterparts of
ligninases have not yet been found, although distinct-
ive intracellular enzymes catalysing all of the above
reactions except cleavage of intermonomeric connec-
tions have been described for low-molecular-weight
substrates.
An additional challenge for potential ligninolytic mi-
croorganisms is the need to gain access to the sub-
stfate by penetration of plant tissues. Fungi, as well as
646 Enzyme Microb. Technol., 1988, vol. 10, November © 1988 Butterworth Publishers