Microbial Degradation of Free and Halogenated Estrogens in River Water-Sediment Microcosms

Abstract

Halogenated estrogens are formed during chlorine-based wastewater disinfection and have been detected in wastewater treatment plant effluent; however, very little is known about their susceptibility to biodegradation in natural waters. To better understand the biodegradation of free and halogenated estrogens in a large river under environmentally relevant conditions, we measured estrogen kinetics in aerobic microcosms containing water and sediment from the Willamette River (OR, USA) at two concentrations (50 and 1250 ng L^-1). Control microcosms were used to characterize losses due to sorption and other abiotic processes, and microbial dynamics were monitored using 16S rRNA gene sequencing and ATP. We found that estrogen biodegradation occurred on timescales of hours to days and that in river water spiked at 50 ng L^-1 half-lives were significantly shorter for 17β-estradiol (t_1/2,bio = 42 ± 3 h) compared to its monobromo (t_1/2,bio = 49 ± 5 h), dibromo (t_1/2,bio = 88 ± 12 h), and dichloro (t_1/2,bio = 98 ± 16 h) forms. Biodegradation was also faster in microcosms with high initial estrogen concentrations as well as those containing sediment. Free and halogenated estrone were important transformation products in both abiotic and biotic microcosms. Taken together, our findings suggest that biodegradation is a key process for removing free estrogens from surface waters but likely plays a much smaller role for the more highly photolabile halogenated forms.

Keywords: biodegradation; estrogen; halogenated estrogen; kinetics; oxidation; river water; sorption; transformation product.

Figure 1

Representative estrogen kinetics for biotic (squares) and abiotic (diamonds) river water microcosms (BD-1907) with sediment (ESH; filled symbols) and without sediment (EH; open symbols) spiked with E2 at 1250 ng L^–1 after normalization to the internal standard, time zero, and the abiotic control (EH only). Modeled fits (shown in gray) were determined by non-linear least squares regression according to the procedure described in the Supporting Information. Standard errors for modeled parameters are presented in Tables 1 and S5.

Figure 2

Estrogen biodegradation (BD-1906) in river water-only microcosms spiked at 50 ng L^–1 after normalization to the internal standard, time zero, and the abiotic control. Photolysis kinetics were determined under ambient solar irradiance on 21 May–14 June 2018 using filtered (0.45 μm) water from the Willamette River (pH 7.6) spiked with individual estrogens (1 mg L^–1; no co-solvent). These photolysis data are presented in the Supporting Information along with a description of the effects of initial concentration, tube geometry, and light screening in river water. Photolysis methods are described in detail in Milstead et al. (2018).

Figure 3

Free and halogenated estrogen biodegradation (BD-1907) in river water-only microcosms spiked at 1250 ng L^–1 (EH) and 50 ng L^–1 (EL) after normalization to the internal standard, time zero, and the abiotic control.

Figure 4

Representative estrogen kinetics (BD-1907) for biotic (squares) and abiotic (diamonds) river water microcosms with sediment (ESH; filled symbols) and without sediment (EH; open symbols) spiked with E2 at 1250 ng L^–1. The concurrent growth and decay of E1 (blue), a transformation product of E2 (orange), was modeled according to the procedure described in the Supporting Information. Similar behavior was observed for diBrE2, including the growth and decay of diBrE1 (data not shown). Quantitation employed an internal standard (E2-d4) normalized calibration approach.