Abstract
Toxic organohalogen pollutants produced as by-products of industrial processes, such as chloroform and polychlorinated dibenzo-p-dioxins, also have significant natural sources. A substantial terrestrial source of halogenated organics originates from fungal decay of wood and leaf litter. Here we show that the lignicolous basidiomycete Phellinus badius deposits up to 30,000 mg of the halogenated metabolite drosophilin A methyl ether (DAME, tetrachloro-1,4-dimethoxybenzene) per kilogram of decayed heartwood in the mesquite Prosopis juliflora. DAME occurs as clusters of glassy crystals up to 1 mm long within the decayed heartwood. In addition, the Phellinus badius basidiocarps contain an average of 24,000 mg DAME/kg dried fruiting body, testifying to the significant translocation and accumulation of Cl accompanied by DAME biosynthesis. The high DAME concentrations attest to the substantial Cl content of the heartwood, which averages near 5,000 ppm, with Cl/K near 1:1, consistent with an inorganic chloride precursor. Phellinus badius has a circumglobal distribution in the tropics and subtropics, where it is widely distributed on hardwoods and commonly associated with decay of mesquite. There is the potential for extensive DAME formation within decayed heartwood worldwide given the extensive range of Phellinus badius and its propensity to form DAME within mesquites. Further, DAME production is not limited to Phellinus badius but occurs in a range of lignicolous basidiomycetes, suggesting a significant natural reservoir for this chloroaromatic with potential environmental implications.
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References
Anchel M (1952) Identification of drosophilin A as a p-methoxy-tetrachlorophenol. J Am Chem Soc 74:2943
Bailey RE (2001) Global hexachlorobenzene emissions. Chemosphere 43:167–182. doi:10.1016/s0045-6535(00)00186-7
Boerjan W, Ralf J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546
Dai YC, Zhou LW, Cui BK, Chen YQ, Decock C (2010) Current advances in Phellinus sensu lato: medicinal species, functions, metabolites and mechanisms. Appl Microbiol Biotechnol 87:1587–1593. doi:10.1007/s00253-010-2711-3
de Jong E, Field JA (1997) Sulfur tuft and turkey tail: biosynthesis and biodegradation of organohalogens by basidiomycetes. Annu Rev Microbiol 51:375–414. doi:10.1146/annurev.micro.51.1.375
de Jong E, Field JA, Spinnler HE, Wijnberg J, Debont JAM (1994) Significant biogenesis of chlorinated aromatics by fungi in natural environments. Appl Environ Microbiol 60:264–270
Dominguez XA, Butruille SD, Gomez-Para F, Reyes C (1972) Isolation of 1,4-dimethoxy-2,3,5,6-tetrachlorobenzene and lactone from Fomes robiniae. Anales De Quimica-Int Ed 68:917
Field JA, Verhagen FJM, de Jong E (1995) Natural organohalogen production by basidiomycetes. Trends Biotechnol 13:451–456. doi:10.1016/s0167-7799(00)89001-0
Gilbertson RL (1979) The genus Phellinus (Aphyllophorales: Hymenochaetaceae) in western North America. Mycotaxon 9:51–89
Gilbertson RL, Burdsall HHJ, Canfield ER (1976) Fungi that decay mesquite in southern Arizona. Mycotaxon 3:487–551
Gribble GW (1998) Naturally occurring organohalogen compounds. Acc Chem Res 31:141–152. doi:10.1021/ar9701777
Gribble GW (2012) Recently discovered naturally occurring heterocyclic organohalogen compounds. Heterocycles 84:157–207. doi:10.3987/rev-11-sr(p)5
Harper DB (1994) Biosynthesis of halogenated methanes. Biochem Soc Trans 22:1007–1011
Harper DB, Kennedy JT, Hamilton JTG (1988) Chloromethane biosynthesis in poroid fungi. Phytochemistry 27:3147–3153. doi:10.1016/0031-9422(88)80017-7
Hiebl J, Lehnert K, Vetter W (2011) Identification of a fungi-derived terrestrial halogenated natural product in wild boar (Sus scrofa). J Agric Food Chem 59:6188–6192. doi:10.1021/jf201128r
Hsu C-S, Suzuji M, Yamada Y (1971) Chemical constituents of fungi I 1,4-dimethoxy-2,3,5,6-tetrachlorobenzene (O-Drosophilin A) from Phellinus yucatensis. Chem Abstr 75a:115864a
Kavanagh F, Hervey A, Robbins WJ (1952) Antibiotic substances from basidiomycetes. 9. Drosophila substrata - (Batsch Ex Fr) Quel. Proc Natl Acad Sci U S A 38:555–560. doi:10.1073/pnas.38.7.555
Khalil MAK et al (1999) Natural emissions of chlorine-containing gases: reactive chlorine emissions inventory. J Geophys Res-Atmos 104:8333–8346. doi:10.1029/1998jd100079
Lavric ED, Konnov AA, De Ruyck J (2004) Dioxin levels in wood combustion—a review. Biomass Bioenergy 26:115–145. doi:10.1016/s0961-9534(03)00104-1
Lee D et al (2011) Screening of Phellinus linteus, a medicinal mushroom, for anti-viral activity. J Korean Soc Appl Biol Chem 54:475–478. doi:10.3839/jksabc.2011.073
Leri AC, Myneni SCB (2010) Organochlorine turnover in forest ecosystems: the missing link in the terrestrial chlorine cycle. Global Biogeochem Cycles 24. doi:10.1029/2010gb003882
Leri AC, Marcus MA, Myneni SCB (2007) X-ray spectromicroscopic investigation of natural organochlorine distribution in weathering plant material. Geochim Cosmochim Acta 71:5834–5846. doi:10.1016/j.gca.2007.09.001
Meera CR, Janardhanan KK (2012) Antitumor activity of a polysaccharide-protein complex isolated from a wood-rotting polypore macro fungus Phellinus rimosus (Berk). Pilat J Environ Pathol Toxicol Oncol 31:223–232
Milliken CE, Meier GP, Sowers KR, May HD (2004) Chlorophenol production by anaerobic microorganisms: transformation of a biogenic chlorinated hydroquinone metabolite. Appl Environ Microbiol 70:2494–2496. doi:10.1128/aem. 70.4.2494-2496.2004
Öberg G, Bastviken D (2012) Transformation of chloride to organic chlorine in terrestrial environments: variability, extent, and implications. Crit Rev Environ Sci Technol 42:2526–2545. doi:10.1080/10643389.2011.592753
Öberg G, Brunberg H, Hjelm O (1997) Production of organically-bound chlorine during degradation of birch wood by common white-rot fungi. Soil Biol Biochem 29:191–197. doi:10.1016/s0038-0717(96)00242-8
Ortiz-Bermudez P, Srebotnik E, Hammel KE (2003) Chlorination and cleavage of lignin structures by fungal chloroperoxidases. Appl Environ Microbiol 69:5015–5018. doi:10.1128/aem. 69.8.5015-5018.2003
Ortiz-Bermúdez P, Hirth KC, Srebotnik E, Hammel KE (2007) Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc Natl Acad Sci U S A 104:3895–3900. doi:10.1073/pnas.0610074104
Řanda Z, Kučera J (2004) Trace elements in higher fungi (mushrooms) determined by activation analysis. J Radioanal Nucl Chem 259:99–107
Redon PO, Abdelouas A, Bastviken D, Cecchini S, Nicolas M, Thiry Y (2011) Chloride and organic chlorine in forest soils: storage, residence times, and influence of ecological conditions. Environ Sci Technol 45:7202–7208. doi:10.1021/es2011918
Reina RG, Leri AC, Myneni SCB (2004) Cl K-edge X-ray spectroscopic investigation of enzymatic formation of organochlorines in weathering plant material. Environ Sci Technol 38:783–789. doi:10.1021/es0347336
Rudawska M, Leski T (2005) Macro- and microelement contents in fruiting bodies of wild mushrooms from the Notecka forest in west-central. Poland Food Chem 92:499–506. doi:10.1016/j.foodcham.2004.08.017
Schwandner FM, Seward TM, Gize AP, Hall K, Dietrich VJ (2013) Halocarbons and other trace heteroatomic organic compounds in volcanic gases from Vulcano (Aeolian Islands, Italy). Geochim Cosmochim Acta 101:191–221. doi:10.1016/j.gca.2012.10.004
Sharifi MR, Nilsen ET, Rundel PW (1982) Biomass and net primary production of Prosopis glandulosa (Fabaceae) in the Sonoran desert of California. Am J Bot 69:760–767. doi:10.2307/2442966
Singh P, Rangaswa S (1966) Occurrence of O-methyl-drosophilin A in Fomes fastuosus. Lev Tetrahedron Lett 1229
Taylor MJ (2006) Biomass in the borderlands: charcoal and firewood production in Sonoran Ejidos. J Southwest 48:63–90
Teunissen PJM, Swarts HJ, Field JA (1997) The de novo production of drosophilin A (tetrachloro-4-methoxyphenol) and drosophilin A methyl ether (tetrachloro-1,4-dimethoxybenzene) by ligninolytic basidiomycetes. Appl Microbiol Biotechnol 47:695–700
van Eijk GW (1975) Drosophilin, a methyl ether from Mycena megaspora. Phytochemistry 14:2506. doi:10.1016/0031-9422(75)80375-x
Verhagen FJM, Swarts HJ, Wijnberg J, Field JA (1998) Organohalogen production is a ubiquitous capacity among basidiomycetes. Chemosphere 37:2091–2104. doi:10.1016/s0045-6535(98)00272-0
Vogt KA, Edmonds RL (1980) Patterns of nutrient concentration in basidiocarps in western Washington Canadian. J Botany Rev Can Bot 58:694–698
Wieczorek MW (1980) Structure of 2,3,5,6-tetrachloro-1,4-dimethoxybenzene. Acta Crystallogr Sect B: Struct Sci 36:1515–1517. doi:10.1107/s0567740880006462
Winterton N (2000) Chlorine: the only green element—towards a wider acceptance of its role in natural cycles. Green Chem 2:173–225. doi:10.1039/b003394o
Yokouchi Y, Saito T, Ishigaki C, Aramoto M (2007) Identification of methyl chloride-emitting plants and atmospheric measurements on a subtropical island. Chemosphere 69:549–553. doi:10.1016/j.chemosphere.2007.03.028
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We wish to acknowledge the comments and support from two anonymous reviewers. The authors gratefully acknowledge the use of facilities within the LeRoy Eyring Center for Solid State Sciences at Arizona State University.
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Communicated by: Sven Thatje
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Garvie, L.A.J., Wilkens, B., Groy, T.L. et al. Substantial production of drosophilin A methyl ether (tetrachloro-1,4-dimethoxybenzene) by the lignicolous basidiomycete Phellinus badius in the heartwood of mesquite (Prosopis juliflora) trees. Sci Nat 102, 18 (2015). https://doi.org/10.1007/s00114-015-1268-5
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DOI: https://doi.org/10.1007/s00114-015-1268-5