Aerobic and Anaerobic Transformations of Pentachlorophenol in Wetland Soils

Strategies to enhance biotransformation of pentachlorophenol (PCP) in a spectrum of wetland soils were investigated under laboratory conditions, which included manipulations of electron acceptors and donors, and PCP concentrations. Maximum transformation rates were found at PCP concentrations <10 jxA/ (methanogenic conditions) and >6 \iM to >23 \s,M (aerobic conditions). Differences in PCP toxicity and sorption among soils and treatments were largely governed by the activities of microbial groups. Within this concentration range, transformation was observed in soils under aerobic and methanogenic conditions, but was inhibited under denitrifying and SOa -reducing conditions. Aerobic PCP transformation initially produced small amounts of pentachloroanisole (PCA). However >75% of both chemicals disappeared in 30 d from five soils. Measured soil properties were not significantly correlated to aerobic transformation rates. Under methanogenic conditions, PCP was reductively dechlorinated to yield a mixture of tetra-, tri-, and dichlorophenols in eight soils, with rates strongly correlated to measures of electron donor supply (total C, N, organic C mineralization rates) and microbial biomass. Addition of protein-based electron donors enhanced reductive dechlorination in a soil low in organic matter and microbial biomass. Results demonstrated the widespread occurrence of PCP transforming microorganisms in soils, which may be promoted by manipulating environmental conditions. C of the environment with polychlorinated phenols (CPs) is of global concern because of their widespread distribution and universal toxicity to life (Escher et al., 1996; ATSDR, 1998). The most common usage of CPs is treatment of wood against fungi and insects, but other sources include production from chlorine bleaching of pulp (Kringstad and Lindstrom, 1984), combustion of organic matter and municipal solid waste (Kanters et al., 1996), and partial transformation of phenoxy pesticides such as 2,4-D and 2,4,5-T (Mikesell and Boyd, 1985). Chlorophenols that enter nontarget upland, wetland, and aquatic environments associate with colloidal and particulate matter and, if not photodegraded, eventually settle onto surface soils (Shiu et al., 1994). There they may be biodegraded, depending on whether degrading microorganisms are present and whether appropriate conditions exist for expression of this activity. There is still much controversy about whether the presence of microbial populations or environmental conditions limE.M. D'Angelo, Soil & Water Biochemistry Lab., Dep. of Agronomy, Univ. of Kentucky, N-122 Agricultural Sci. Bldg. North, Lexington, KY 40546-0091; and K.R. Reddy, Univ. of Florida Wetland Biogeochemistry Lab., Soil and Water Sci. Dep., 106 Newell Hall, P.O. Box 110510, Gainesville, FL 32611-0510. Florida Agric. Exp. Stn. Journal Ser. no. R-07269. Mention of a specific product or trade name does not constitute endorsement of the University of Florida to the exclusion of others. Received 11 Mar. 1999. ""Corresponding author ([email protected]). Published in Soil Sci. Soc. Am. J. 64:933-943 (2000). its degradation of chlorinated toxic organic chemicals (Renner, 1998). Historically, environmental persistence of PCP and less chlorinated phenols has been attributed to the absence of degrading populations of microorganisms. However, increasing numbers of observations in diverse habitats indicate that transformation potential is widespread, but is manifested only under favorable environmental conditions. Important variables include temperature (Kohring et al., 1989), availability of electron acceptors (Haggblom et al., 1993), electron donors (Kuwatsuka and Igarashi, 1975; Chang et al., 1996), nutrients (Mileski et al., 1988; Schmidt, 1996), and toxic metals (Kuo and Genther, 1996). In wetland and aquatic systems, these properties are often present as gradients resulting in a continuum of microbial activities. In aerobic soils, transformation of PCP by Flavobacterium and Rhodococcus spp., among others, proceeds though sequential hydroxylation and reductive removal of chlorine substituents yielding poly-hydroxybenzene compounds that are eventually mineralized to CO2 (Uotila et al., 1995; Xun et al., 1992). Several Rhodococcus spp. also methylate PCP resulting in production of volatile PCA (Middelorp et al., 1990). Several species of fungi mineralize PCP via ligninase enzymes (Mileski et al., 1988) and produce extracellular enzymes that polymerize CPs with humic substances (Bhandari et al., 1996; Ruttimann-Johnson and Lamar, 1997). In anaerobic soils, the pathway for anaerobic transformation of PCP is sequential replacement of chlorines by hydrogen (reductive dechlorination), leading to phenol, benzoate, acetate, CO2 and CH4 (Kuwatsuka and Igarashi, 1975; Zhang and Wiegel, 1990). To date, a few anaerobic isolates having the capacity for reductive dechlorination of PCP have been discovered, and these often gain energy by coupling this process to oxidative phosphorylation (Mohn and Tiedje, 1991; Loffler et al., 1996). The resultant lesser chlorinated products from reductive dechlorination likely function as carbon and energy sources for those aerobic and anaerobic microorganisms involved (Haggblom and Young, 1990). Predicting the persistence of microbially transformed toxic organic contaminants is currently hindered by limited knowledge of the influence of environmental variables on degradation rates (Hart, 1996). Previous experiments in numerous wetland soils, however, have demonstrated that heterotrophic microbial activities were related to soil properties (D'Angelo and Reddy, 1999), suggesting that similar relationships may also exist for transformation of toxic organic chemicals. The Abbreviations: A, aqueous concentration; CPs, polychlorinated phenols; DCP, dichlorophenol; EC;0, effective concentration; Ka, acid dissociation constant; Kp, linear sorption coefficient; PCA pentachloroanisole; PCP, pentachlorophenol; T, total soil concentration; TCP, trichlorophenol; TeCP, tetrachlorophenol.