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Microbial degradation of aromatic compounds — from one strategy to four

Nature Reviews Microbiology volume 9, pages 803–816 (2011)Cite this article

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Key Points

  • Aromatic compounds are common growth substrates for microorganisms and are also prominent environmental pollutants. The crucial step in their degradation is to overcome the huge resonance energy that stabilizes the aromatic ring. The microbial degradation of aromatic compounds includes a great variety of mechanisms and chemical reactions, some of which have only rare counterparts in organic chemistry.

  • The classical strategy for aromatic-ring cleavage, which is restricted to aerobic organisms, comprises an attack by oxygenases that hydroxylate and finally cleave the ring with the help of activated molecular oxygen (O2). However, three additional strategies exist that are based on completely different ring activation mechanisms and use CoA thioesters and ring cleavage by hydrolysis.

  • The first strategy depends on the presence of O2 and uses monooxygenases of the class I di-iron protein family. These enzymes are epoxidases that form non-aromatic ring-epoxides of benzoyl-CoA and phenylacetyl-CoA, compounds that are further metabolized by ring hydrolysis.

  • The other two strategies are O2 independent, involve the reduction of the aromatic ring and, under anoxic conditions, convert most aromatic substrates into benzoyl-CoA as a central intermediate.

  • One of the O2-independent strategies for aromatic-ring cleavage is used by facultative anaerobic bacteria when they are growing phototrophically or during anaerobic respiration. In these circumstances, these bacteria reduce benzoyl-CoA by an ATP-driven benzoyl-CoA reductase that hydrolyses two molecules of ATP.

  • By contrast, during low-energy-yield anaerobic respiration or fermentation, strictly anaerobic bacteria use a different class of benzoyl-CoA reductase that is ATP independent. The low redox potential that is required for benzoyl-CoA reduction is probably achieved by a process called electron bifurcation. Electrons from two reduced ferredoxins are split via a flavin cofactor into low- and high-redox-potential electrons. Low-redox-potential electrons may reduce the aromatic ring, whereas high-redox-potential electrons may reduce NAD+.

Abstract

Aromatic compounds are both common growth substrates for microorganisms and prominent environmental pollutants. The crucial step in their degradation is overcoming the resonance energy that stabilizes the ring structure. The classical strategy for degradation comprises an attack by oxygenases that hydroxylate and finally cleave the ring with the help of activated molecular oxygen. Here, we describe three alternative strategies used by microorganisms to degrade aromatic compounds. All three of these methods involve the use of CoA thioesters and ring cleavage by hydrolysis. However, these strategies are based on different ring activation mechanisms that consist of either formation of a non-aromatic ring-epoxide under oxic conditions, or reduction of the aromatic ring under anoxic conditions using one of two completely different systems.

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Figure 1: Environmental sources of aromatic compounds.
Figure 2: Peripheral (upper) pathways in the degradation of aromatic compounds.
Figure 3: The β-ketoadipate pathway and ring-cleaving dioxygenases.
Figure 4: Aerobic degradation of benzoyl-CoA and phenylacetyl-CoA.
Figure 5: Anaerobic degradation of benzoyl-CoA.
Figure 6: Anaerobic degradation of aromatic hydrocarbons.

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Acknowledgements

The authors gratefully acknowledge the funding of their work by the Deutsche Forschungsgemeinschaft and the contributions of numerous co-workers over many years.

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Authors and Affiliations

  1. Mikrobiologie, Fakultät Biologie, Universität Freiburg, Schänzlestr. 1, D-79104, Freiburg, Germany

    Georg Fuchs

  2. Institut für Biochemie, Universität Leipzig, Brüderstr. 34, D-04103, Leipzig, Germany

    Matthias Boll

  3. Mikrobiologie, Fachbereich Biologie, Universität Marburg, Karl-von-Frisch-Str. 8, D-35043, Marburg, Germany

    Johann Heider

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  1. Georg Fuchs
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Glossary

Humus

Any organic matter in soil (particularly decayed lignin) that has reached a point of stability such that it will break down no further and might, if conditions do not change, essentially remain as it is for a long time.

Mesomeric structures

Two or more structures that can be assigned to a single molecule, neither of which is capable of describing all the known properties of the compound. The actual structure is considered to be a resonance hybrid, or an intermediate of these structures, and these structures are therefore also known as resonating structures.

π bond

A chemical bond that results from the overlap of atomic p orbitals that are in contact through two areas of overlap. π bonds are more diffuse than σ bonds. Molecular fragments joined by a π bond cannot rotate around that bond without breaking it.

p orbitals

Dumbbell-shaped regions describing where an electron can be found, within a certain degree of probability.

'Triplet' state

The ground state of the oxygen molecule. The electron configuration of O2 has two unpaired electrons occupying two degenerate molecular orbitals with four different spin states, of which the triplet states are energetically more favourable. This unusual electron configuration prevents molecular oxygen from reacting directly with many other molecules.

Birch reduction

A widely used tool in synthetic organic chemistry, for the de-aromatization of aromatic rings by reduction, as first reported in 1944 by Arthur Birch. It proceeds via alternating electron transfer and protonation steps, and it usually forms cyclohexa-1,4-dienes without further reduction.

Electron bifurcation

An enzymatic process in which a thermodynamically unfavourable redox reaction is driven by a thermodynamically favoured one.

Catabolite repression

A control system that allows bacteria to adapt quickly to use a preferred (that is, able to be metabolized rapidly) carbon and energy source first. This is usually achieved through inhibition of the synthesis of enzymes involved in catabolism of carbon sources other than the preferred one.

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Fuchs, G., Boll, M. & Heider, J. Microbial degradation of aromatic compounds — from one strategy to four. Nat Rev Microbiol 9, 803–816 (2011). https://doi.org/10.1038/nrmicro2652

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