Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production

Abstract

Soils and decayed plant litter contain significant quantities of chlorinated aromatic polymers that have a natural but largely unknown origin. We used cupric oxide ligninolysis coupled with gas chromatography/mass spectrometry to show that Curvularia inaequalis, a widely distributed litter ascomycete, chlorinated the aromatic rings of lignin in wood that it was degrading. In aspen wood decayed for 24 weeks, two chlorolignin fragments, 5-chlorovanillin and 2-chlorosyringaldehyde, were each found at Ϸ10 g/g of wood (dry weight). These levels resemble those of similar structures generally found in unpolluted environmental samples. Fractionation of the extractable proteins followed by tandem mass spectrometric analysis showed that the colonized wood contained a previously described C. inaequalis chloroperoxidase that very likely catalyzed lignin chlorination. Chlorolignin produced by this route and humus derived from it are probably significant components of the global chlorine cycle because chloroperoxidase-producing fungi are ubiquitous in decaying lignocellulose and lignin is the earth's most abundant aromatic substance.chloroperoxidase ͉ humus ͉ hypochlorous acid ͉ Pleosporales ͉ soil

X-ray spectromicroscopic investigation of natural organochlorine distribution in weathering plant material

“…The post-edge spectral features in F. oxysporum-produced aromatic Cl org bear a distinct resemblance to those in the aromatic Cl org hotspots observed in weathered leaves from the forest floor. This result further implicates fungi in the production of aromatic Cl org in decaying plant material, which resonates with recent evidence that fungi chlorinate aromatic rings as they degrade lignin (Ortiz-Bermú dez et al, 2007).…”

“…Commercial chloroperoxidase (CPO), a haloperoxidase enzyme isolated from source fungi, has proved capable of chlorinating non-specific phyto-organic molecules (Reina et al, 2004) and fulvic acid moieties . Ligninolytic ascomycetes fungi display CPO activity and chlorinate aromatic lignin structures as they break down plant material (Ortiz-Bermú dez et al, 2007). Such fungi are omnipresent in soil systems and probably make significant contributions to the global Cl org pool.…”

Vanadium haloperoxidases: From the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies

“…The fungus C. inaequalis is able to chlorinate aromatic rings of lignin in wood during the degradation process and this action is likely to be due to the presence of VCPO enzymes [86]. The VHPO-based biofilm control has been also explored for medical purposes: VCPO from C. inaequalis has an antimicrobial action on Enterococcus faecalis biofilms [87].…”

Technical Note: Reactivity of C1 and C2 organohalogens formation – from plant litter to bacteria

“…Abiotically, aliphatic volatile organohalogens were released from senescent and dead leaves (Hamilton et al, 2003), Fe-oxyhydroxide and halide containing soil or sediment (or with H 2 O 2 ; Fahimi et al, 2003;Huber et al, 2009), and emissions from savannah fires, volcanoes, hydrothermal sources, and salt mines (Weissflog et al, 2005;Gribble, 2010). Biotically, enzymes like haloperoxidases and halogenases widespread in soils and oceans are thought to contribute the major sources of environmental organohalogens (Nightingale et al, 1995;Hoekstra et al, 1998;Öberg, 2002;Reddy et al, 2002;Ortiz-Bermudez et al, 2007;Blasiak and Drennan, 2009;Wagner et al, 2009). Although many efforts have identified a wide range of natural organic matters (NOMs) from soils, plant and animal debris, algae, and fungi as precursors of organohalogens (Nightingale et al, 1995;Hoekstra et al, 1998;Keppler et al, 2000;Myneni, 2002;Fahimi et al, 2003;Hamilton et al, 2003;Huber et al, 2009), there is great uncertainty associated with source inventories and fluxes for C1/C2 organohalogens, with few taking bacteria precursors into account.…”

“…Among different natural halogenation routes, halogenation of organic matter by reactive halogen species (e.g., OCl − generated by chloroperoxidase) is the most common proposed route for natural organohalogen generation (Öberg, 2002;Ortiz-Bermudez et al, 2007;Wagner et al, 2009). In this study, seven strains of common bacteria (B1: Acinetobacter junii; B2: Aeromonas hydrophila; B3: Bacillus cereus; B4: Bacillus subtilis; B5: Escherichia coli; B6: Shigella sonnei; and B7: Staphylococcus sciuri) at stationary phase and nine monomers of bacterial materials were selected to explore the maximum potential to form organohalogens by direct halogenation (using NaOCl solution as in Albers et al, 2011).…”