Perfluorinated Organic Compounds and Polybrominated Diphenyl Ethers Compounds
Evidence for photochemical and microbial debromination of polybrominated diphenyl ether flame...
-
Upload
ben-greenfield -
Category
Documents
-
view
15 -
download
2
description
Transcript of Evidence for photochemical and microbial debromination of polybrominated diphenyl ether flame...
1
Evidence for photochemical and microbial debromination of polybrominated 1
diphenyl ether flame retardants in San Francisco Bay sediment 2
3
Lisa A. Rodenburg1*, Qingyu Meng2, Don Yee3, and Ben K. Greenfield3,4 4
1 Department of Environmental Sciences, Rutgers University, 14 College Farm 5
Road, New Brunswick, NJ 08901, USA 6
2School of Public Health, Rutgers University, Piscataway, New Jersey 08854, United States 7
3San Francisco Estuary Institute, 4911 Central Avenue, Richmond, CA 94804 8
4Current affiliation: Environmental Health Sciences Division, School of Public Health, 9
University of California, Berkeley, 50 University Hall #7360, Berkeley, CA 94720-7360 10
*Corresponding author. Phone 732-932-9800 x 6218, Fax 732-932-8644, email 11
13
2
ABSTRACT 14
Brominated diphenyl ethers (BDEs) are flame retardant compounds that have been classified as 15
persistent organic pollutants under the Stockholm Convention and targeted for phase-out. 16
Despite their classification as persistent, PBDEs undergo debromination in the environment, via 17
both microbial and photochemical pathways. We examined concentrations of 24 PBDE 18
congeners in 233 sediment samples from San Francisco Bay using Positive Matrix Factorization 19
(PMF). PMF analysis revealed five factors, two of which contained high proportions of 20
congeners with two or three bromines, indicating that they are related to debromination 21
processes. One of the factors included PBDE 15 (4,4’-dibromo diphenyl ether, comprising 20% 22
of the factor); the other included PBDE 7 (2,4-dibromo diphenyl ether; 12%) and PBDE 17 23
(2,2’,4-tribromo diphenyl ether; 16%). The debromination processes that produce these 24
congeners are probably photochemical debromination and anaerobic microbial debromination, 25
although other processes could also be responsible. Together, these two debromination factors 26
represent about 8% of the mass and 13% of the moles of PBDEs in the data matrix, suggesting 27
that PBDEs undergo measurable degradation in the environment. 28
29
Key words: photolysis, debromination, monitoring, factor analysis, California, flame retardant 30
31
1 INTRODUCTION 32
Brominated diphenyl ethers (BDEs) are flame retardant compounds that have been 33
widely used in consumer products since the 1970s, exhibit elevated concentrations in seafood 34
and indoor dust, and may pose human health hazards at environmentally relevant concentrations 35
(Domingo, 2012). As a result, PBDEs have been classified as persistent organic pollutants 36
3
(POPs) under the Stockholm Convention and are targeted for phase-out (United Nations 37
Environment Program, 2009). Despite their classification as persistent, PBDEs undergo 38
debromination via microbial and photochemical pathways that have been studied under 39
laboratory conditions, but as yet there is little understanding of their importance for the 40
environmental fate of PBDEs. 41
The photolysis of PBDEs, studied with multiple light sources and media, exhibits 42
characteristic pathways and breakdown products (Sanchez-Prado et al., 2006; Fang et al., 2008; 43
Sanchez-Prado et al., 2012; Wei et al., 2013 and references therein). Several researchers (Fang 44
et al., 2008; Sanchez-Prado et al., 2012; Wei et al., 2013) have demonstrated that during 45
photolysis, removal of bromines in the ortho position predominates. PBDE 15 (4,4’-46
dibromodiphenyl ether) is a major photolysis product, with PBDE 17 (2,2',4-tribromodiphenyl 47
ether) sometimes reported as a minor product (Sanchez-Prado et al., 2012; Wei et al., 2013). 48
Ahn et al. (2006) studied PBDE photolysis on clays, metal oxides, and sediments and concluded 49
that the photolysis pathways were largely matrix independent. 50
Although the regiospecificity of microbial debromination of PBDEs is more complicated, 51
certain breakdown products are observed. Using a biomimetic system, Tokarz et al. (2008) 52
noted that PBDEs 17 (2,2’,4-tribromo diphenyl ether) and 28 (2,4,4’-tribromo diphenyl ether) 53
were major microbial debromination products of high molecular weight PBDEs in anaerobic 54
sediment. Tokarz et al. (2008) also indicated that although microbial debromination at the ortho 55
positions is possible, removal of the meta and para bromines predominates, especially for heavy 56
congeners. Similarly, Robrock et al. (2008) and Ding et al. (2013) found that debromination of 57
PBDEs by several cultures preferentially removed bromines at the meta and para positions, with 58
formation of PBDE 17 as a major product. La Guardia et al. (2007) observed evidence of 59
4
microbial debromination of PBDEs in sewage sludge and near wastewater outfalls. They 60
measured PBDE 17 but could not detect PBDE 15 in sewage sludge. Davis et al. (2012) also 61
detected PBDE 17 in biosolids. In contrast, Lee et al. (2011) studied the debromination of PBDE 62
by a coculture consisting of Dehalococcoides and Desulfovibrio species, and found that 63
debromination at the ortho position is preferred, with significant amounts of PBDE 15 formed. 64
This echoes the regiospecificity of the microbial dechlorination of polychlorinated biphenyls 65
(PCBs): dechlorination at the meta and para positions is preferred, but chlorines at the ortho 66
position can be removed by some strains of bacteria (Bedard, 2003). For the PBDEs, it is not 67
clear which set of pathways predominates in the environment, and indeed different 68
regiospecificity might be observed in different environments. 69
The purpose of this work was to use factor analysis to examine the importance of these 70
debromination processes in the environment. Data collected by the Regional Monitoring 71
Program for Water Quality in the San Francisco Estuary (RMP) were analyzed using Positive 72
Matrix Factorization (PMF) (Paatero and Tapper, 1994). The RMP data set is a good choice for 73
this investigation because it includes measurements of 50 PBDE congeners using high-resolution 74
mass spectrometry in hundreds of sediment samples collected in San Francisco Bay (Oram et al., 75
2008; Klosterhaus et al., 2012). PMF is an advanced factor analysis method, described in detail 76
by Paatero and Tapper (1994). Briefly, PMF defines the sample matrix as product of two 77
unknown factor matrices with a residue matrix: 78
EGFX += (1) 79
The sample matrix (X) includes n observed samples and m chemical species. F is a matrix of p 80
chemical profiles. The G matrix describes the contribution of each factor to any given sample, 81
5
while E is the matrix of residuals. The PMF solution (i.e., G and F matrices) is obtained by 82
minimizing the objective function Q through the iterative algorithm: 83
2
1 1
)/(∑∑= =
=n
i
m
jijij seQ (2) 84
Q is the sum of the squares of the difference (i.e., eij) between the observations (X) and the model 85
(GF), weighted by the measurement uncertainties (sij). 86
PMF has several advantages over simpler factor analysis tools such as Principle 87
Components Analysis (PCA). PMF allows only positive correlations, and because the model 88
input includes a point-by-point uncertainty estimate, PMF allows the inclusion of missing or 89
below detection limit data points, which are assigned an arbitrary concentration and then 90
associated with a high uncertainty. PMF and other similar factor analysis methods have been 91
used to investigate the dehalogenation of PBDEs (Zou et al., 2013) as well as other POPs, 92
including polychlorinated biphenyls (PCBs) (Magar et al., 2005; Bzdusek et al., 2006b; 93
Rodenburg et al., 2010) and polychlorinated dibenzo-p-dioxins and polychlorinated 94
dibenzofurans (PCDD/Fs) (Barabas et al., 2004; Rodenburg et al., 2012). Like all factor analysis 95
methods, however, PMF can only isolate the factors that make up the data set. It is up to the user 96
to use her best judgment to understand what these factors mean. 97
2 METHODS 98
2.1 Study site 99
San Francisco Bay (the Bay, Figure 1) is one of the largest urbanized estuaries in the 100
world, with a surrounding population of 7 million people. Bay hydrology is driven primarily by 101
the tidal influence from the Pacific Ocean and the freshwater inflow from the Sacramento and 102
San Joaquin Rivers, which drain an area of about 150,000 km2 (Cloern, 1996), and enter the Bay 103
6
at its northern end in Suisun Bay (Figure 1). As a result of freshwater inflow and tidal mixing, 104
the northern Bay (Suisun and San Pablo Bays) is relatively well flushed, whereas South Bay is 105
less well flushed (Conomos, 1979). Treated wastewater discharge is released via 31 permitted 106
outfalls distributed Baywide, totaling a dry weather permitted flow into the Bay of 788 MGD. 107
Concentrations of many pollutants, including PBDEs, are highest in Central Bay, South Bay, and 108
Lower South Bay sediment and tend to decline moving northward towards San Pablo and Suisun 109
Bays (Oros et al., 2005; Davis et al., 2007; Klosterhaus et al., 2012). 110
The Regional Monitoring Program for Water Quality in the San Francisco Estuary (RMP) 111
is an ongoing monitoring partnership established in 1993 between a regulatory agency, over 70 112
local regulated entities, and other local stakeholders (e.g., environmental NGOs), administered 113
by an independent scientific organization (Hoenicke et al., 2003). RMP sediment monitoring 114
employs a stratified design, in which eight probabilistic sites are collected annually from each of 115
five Bay segments following a rotating panel design, with seven additional samples collected 116
from fixed monitoring stations (Lowe et al., 2004). Every sample incorporates two to three 117
homogenized subsamples, each collected by 0.1 m2 Kynar ® coated stainless steel Young-118
modified Van Veen grab. Trace clean techniques are employed, including quadruple rinsing of 119
all equipment between each sampling event (SFEI, 2012). Beginning in 2002, fifty PBDE 120
congeners were measured in the sediment by Axys Analytical Services (British Columbia, 121
Canada) using high resolution gas chromatography/mass spectrometry methods equivalent to 122
EPA method 1614A (EPA, 2007). 123
2.2 Data matrix 124
Of the 50 congeners measured, only 24 were above the detection limit in more than 50% 125
of the 403 sediment samples. These 24 congeners were retained for PMF analysis. Only samples 126
7
with fewer than four non-detects were included in analysis. This resulted in 24 congeners 127
measured in 233 samples, with adequate detection limits only occurring in sampling years 2005 128
through 2010. 129
2.3 PMF analysis 130
The data were analyzed using Positive Matrix Factorization (PMF), employing PMF2 131
software (YP-Tekniika KY Co., Helsinki, Finland). 132
PMF computes the error estimate (sij) for each data point (xij) based on the data point and 133
its original error estimate. The present study utilizes the error model (EM) = -14 (Paatero, 2003): 134
),max(),max( ijijijijijijijij yxvyxutS ++= (3) 135
where t is the congener- and sample-specific detection limit, u is the Poisson distribution (here 136
designated as 0), v is the measurement precision, x is the observed data value, and y is the 137
modeled value. The uncertainty matrix was constructed by assigning an uncertainty of 15% to all 138
congeners except those below detection. For values below detection, a value of one-half the 139
detection limit was assigned, and the uncertainty was set to 166% (Brown and Hafner, 2003). 140
Congener and sample-specific detection limits were used to construct the detection limit matrix. 141
142
3 RESULTS AND DISCUSSION 143
In the 233 samples analyzed by PMF, Σ24BDE congener concentrations ranged from 0.16 144
to 54 µg/kg (mean = 4.3 µg/kg; median = 3.3 µg/kg). PBDE 209 was the most abundant 145
congener in 216 of the 233 samples. Congeners with four or fewer bromines comprised between 146
0.3% and 28% of Σ24BDEs (mean = 9.9%; median = 9.5%). These low molecular weight 147
congeners (for example, PBDEs 17 and 28) constitute less than 1% of penta PBDE formulations 148
8
and are not detectable in octa and deca formulations (La Guardia et al., 2006). Their abundance 149
in the majority of samples suggests that debromination processes significantly impact PBDE 150
congener patterns in Bay sediments. 151
A matrix of Pearson’s correlation coefficients (Supporting Information Table S1) reveals 152
that PBDE 209 is correlated with PBDEs 206 and 207, indicative of the commercial deca PBDE 153
formulation. PBDEs 47, 99, and 100 are also correlated, indicative of the penta formulation (La 154
Guardia et al., 2006). PBDEs 15 and 17 are uncorrelated, indicating that they arise from 155
different sources, processes, or locations. 156
3.1 Positive Matrix Factorization 157
Determining the correct number of factors is always a central challenge of factor analysis. 158
A weight of evidence approach, described in the Supplemental Information Text, determined that 159
five factors were appropriate; remaining interpretations focus on the five factor solution. 160
3.2 PMF congener patterns 161
Examining congener patterns, factor 5 is dominated by PBDE 209 with smaller 162
contributions from PBDEs 206, 207, and 208 (Figure 2). PBDE 209 is also dominant in factor 2, 163
present but not dominant in factors 3 and 4, and a minor contributor to factor 1. Factors 1 164
through 4 contain tetra- or less- brominated congeners which are not abundant in commercial 165
PBDE formulations; these likely represent debromination products of higher molecular weight 166
PBDE congeners. 167
Based on comparison with the congener patterns of the commercial PBDE formulations 168
(La Guardia et al., 2006), factor 4 represents penta-BDE formulations such as DE-71 and 169
Bromkal 70-5DE, because it is dominated by PBDEs 47, 99, and 100 (Figure 2). However, 170
factor 4 contains higher proportions of PBDEs 17 (1.8% of total Σ24BDEs in the factor) and 28 171
9
(2.6%) than would be expected from the technical mixtures, since Bromkal 70-5DE contains less 172
than 0.2% of these congeners. This elevated proportion may indicate either debromination or 173
weathering (for example, preferential transport of lower molecular weight congeners). 174
Factor 5 contains 82% of all of the PBDE 209 mass in the data set and more than 75% of 175
the PBDEs 206, 207, and 208 masses (Figure 2), and thus represents the technical deca mixtures, 176
such as Saytex 102E and Bromkal 82-0DE (La Guardia et al., 2006). Factors 2 and 4 contain 177
moderately high proportions of PBDE 209 (Figure 2), accounting for 14% and 4% of the PBDE 178
209 mass, respectively. Notably absent from the resolved factors is anything resembling the 179
technical octa-BDE mixtures. 180
Factor 2 contains congeners that are not present in any of the commercial PBDE 181
mixtures, including dibromo congeners PBDEs 7 and 8 (Figure 2), and 12% of PBDE 17 (as 182
compared to less than 0.1% within the commercial mixtures), suggesting debromination of heavy 183
congeners. However, the major constituents of this factor are PBDE 47, 99, and 100, which are 184
associated with the commercial penta PBDE mixtures, and PBDE 209. We hypothesize that 185
factor 2 represents the weathered PBDE background in the sediments, with traces of both major 186
commercial formulations (penta and deca) and some evidence of debromination. Weathering is a 187
generic term that encompasses many processes, including debromination as well as physical 188
processes such as mixing, partitioning, and preferential transport. The PMF factor analysis 189
identifies congener patterns that co-vary. This can mean that they are produced from the same 190
location or process, or that they are merely transported together. Thus factor 2 may represent 191
BDE congeners that have been transported together despite the fact that they come from several 192
sources and have undergone debromination as well as preferential transport, both of which may 193
alter the original (source) congener patterns. This might indicate that factor 2 is associated with 194
10
an aggregate or secondary source, such as storm water or treated wastewater. Alternatively, it 195
could indicate PBDEs that entered the bay long ago and have had time to undergo a lot of 196
mixing, transport, and degradation. 197
Factors 1 and 3 contain lower molecular weight PBDE congeners that are not present in 198
the commercial PBDE mixtures. Factor 3 represents 5.4% of the mass and 7.8% of the moles of 199
PBDEs in the data set, and contains high proportions of PBDE 17 (16% of Σ24BDEs), PBDE 7 200
(12%) and PBDE 49 (11%) (Figure 2). PBDEs 17 and 49 have been reported as products of 201
microbial debromination of PBDE technical mixtures (Robrock et al., 2008; Tokarz et al., 2008), 202
suggesting that factor 3 indicates microbial debromination. The abundance of PBDE 47 in factor 203
3 is inconclusive, as PBDE 47 is both a major congener in many commercial formulations (La 204
Guardia et al., 2006) and a microbial debromination product (Robrock et al., 2008; Tokarz et al., 205
2008). 206
Factor 1 represents about 3.1% of the mass and 4.9% of the moles of PBDEs in the data 207
set. It contains 20% PBDE 15, which is mostly absent from the other factors (Figure 2), 208
consistent with the lack of correlation between PBDE 15 and 17. Factor 1 also contains PBDEs 209
47, 49, and 66. 210
BDE 15 in Factor 1 has not been reported as a measurable constituent of the commercial 211
formulations, and therefore likely indicates either photochemical or microbial debromination. 212
The case for photolysis rests on the observations of several researchers (Fang et al., 2008; 213
Sanchez-Prado et al., 2012; Wei et al., 2013) who noted PBDE 15 as a major product of 214
photochemical debromination of heavier congeners. PBDEs 47, 49, and 66, present in Factor 1, 215
are all important in the photochemical degradation pathway. Although photolysis is expected to 216
be negligible within surface sediment, it can occur during transport while PBDEs are sorbed to 217
11
suspended clay minerals (Ahn et al., 2006), or while in the gas phase or dissolved in water. In 218
the sediments of the Daliao River Estuary, China, PBDE 15 was abundant at concentrations 219
which were not well correlated with other congeners (Zhao et al., 2011). The authors suggested 220
PBDE 15 formation during atmospheric transport, with atmospheric deposition as the main 221
source to surface sediment. The interpretation of factor 1 as photochemical debromination is 222
also supported by its relatively even distribution across the Bay, as described below. 223
It is also possible that factor 1 indicates microbial debromination that occurs with 224
different regiospecificity than in factor 3. This would imply different bacterial populations and/or 225
environmental conditions for each factor. Since PBDE 15 is the major product of this process, 226
ortho debromination would have to be prevalent in this pathway. As noted above, there is no 227
correlation between PBDEs 15 and 17 across the data matrix. If both congeners represent 228
debromination, this lack of association suggests different locations or transport processes. Since 229
microbial debromination is most likely an anaerobic process, this implies that there are two sets 230
of anaerobic zones distributed throughout the Bay, each producing a very different congener 231
pattern. This seems unlikely. If debromination was observed to occur in a few hot spots, this 232
explanation would be more plausible. 233
A third possibility is that factor 1 or 3 (or both) could indicate debromination by aquatic 234
animals (Stapleton et al., 2004), plants (Wang et al., 2012; Huang et al., 2013), or aerobic 235
bacteria (Deng et al., 2011). For many of these processes, the products have not been measured, 236
or at least the regiospecificity has not been reported, so it is unknown whether they could 237
produce PBDE 15, which requires ortho debromination. Like PBDEs, PCBs can also be 238
degraded in fish, plants, and by aerobic bacteria (Buckman et al., 2006; Field and Sierra-Alvarez, 239
2008; Van Aken et al., 2010), sometimes resulting in dramatic changes in congener patterns. To 240
12
date, however, none of these altered congener patterns has been observed in sediment (Imamoglu 241
et al., 2004; Bzdusek et al., 2006a; Bzdusek et al., 2006b; Soonthornnonda et al., 2011; Praipipat 242
et al., 2013). The total biomass of aquatic animals and plants is likely to be relatively low, 243
compared to microbes, suggesting that they would have limited impact on PCB and PBDE 244
congener patterns on an ecosystem-wide basis. In contrast, microbial dechlorination of PCBs is 245
known to alter PCB congener patterns in sediment (Bzdusek et al., 2006a; Bzdusek et al., 246
2006b). 247
Based on this evidence, we speculate that the most likely explanation of the PMF2 results 248
is that factor 1 indicates photochemical debromination, and factor 3 indicates debromination by 249
anaerobic bacteria, which either occurs in the sediments themselves or in sewers or other 250
environments, with the products transported into and mixed throughout the Bay. Additional 251
evidence is needed to confirm this conjecture, however. Factor analysis alone cannot 252
definitively distinguish between photochemical and microbial debromination because both 253
processes can produce BDEs 15 and 17. 254
3.3 Spatial distribution of factors 255
Factor 1 (photolysis or ortho debromination) concentrations ranged from below detection 256
limits (ND) to 0.61 ng/g (figure 3 panel 1A). The relative contribution of factor 1 to the total 257
(figure 3 panel 1B) was higher for the less urbanized northern Bay segments (San Pablo Bay and 258
Suisun Bay; average 9% contribution to total) than southern Bay segments (Lower South, South, 259
and Central Bays; averaging 2 to 3% contribution to total). This distribution is consistent with 260
the hypothesis that factor 1 results from photolysis in the gas phase and subsequent atmospheric 261
deposition. Specifically, the mass of photodebrominated PBDEs contributed from atmospheric 262
13
deposition would be similar across the Bay, but the relative contribution would be reduced by 263
greater inputs of PBDEs in the southern Bay. 264
Factor 2 exhibited variable concentrations ranging from ND to 4.2 ng/g (Figure 3 panel 265
2A). The fractional contribution of factor 2 was greatest in San Pablo Bay and Central Bay 266
(Figure 3 panel 2B), consistent with our hypothesis that this factor represents a weathered PBDE 267
background. Specifically, the largest PBDE sources likely occur in the South Bay region, with 268
increased mixing and weathering with transport and dispersion away from original sources. 269
Factor 3 (microbial debromination) maximum concentrations were 1.1 ng/g (21% of the 270
total PBDE mass; Figure 3 panels 3A and 3B). The highest fraction of factor 3 was generally 271
seen in South Bay and the lowest fraction in San Pablo Bay. South Bay receives a high 272
proportion of stormwater and treated sewage outfalls, mostly via Lower South Bay, whereas the 273
majority of inflow to San Pablo Bay originates from riverine input (Sacramento and San Joaquin 274
Rivers, via Suisun Bay, and to a lesser extent Napa and Petaluma Rivers). The sewage outfall 275
inputs and lower flushing rates may increase sediment anoxia in the South Bay (Cloern, 1996), 276
potentially promoting microbial dehalogenation. Elevated factor 3 concentrations were not 277
observed in Lower South Bay (where the major outfalls are located), suggesting that 278
debromination prior to discharge within the sewers draining into Lower South Bay may not be a 279
major contributor to microbial debromination products. 280
Concentrations of factor 4 ranged up to 3.8 ng/g and 76% of the Σ24BDEs (Figure 3 panel 281
4A). Concentrations displayed no obvious spatial trend in the Bay, in keeping with the 282
ubiquitous sources of fresh penta-BDE throughout the urban area. However, the fraction of total 283
PBDEs contributed by factor 4 generally increased moving northward from Lower South Bay 284
through Suisun Bay and the Rivers (Figure 3 panel 4B). 285
14
Factor 5 (deca-BDE) concentrations ranged up to 12.4 ng/g (Figure 3 panel 5A). Factor 5 286
was the predominant factor in 138 of the 233 samples, and was most abundant in the Lower 287
South Bay (Figure 3 panel 5B). This distribution was opposite that determined by loading 288
estimates. Oram et al. (2008) considered loads of PBDEs 47 and 209 from the Sacramento-San 289
Joaquin Delta, local tributaries, municipal wastewater, and atmospheric deposition. Oram et al. 290
suggested that PBDE 47 (generally corresponding to factor 4) loads were dominated by 291
wastewater, while PBDE 209 (corresponding to factor 5) loads were dominated by runoff from 292
the Sacramento and San Joaquin Rivers. There are several possible reasons for the discrepancy 293
between the PMF results and the mass budget of Oram et al. First, Oram et al. did not consider 294
some PBDE sources that might be significant, including storm water runoff. More importantly, 295
the PMF analysis considered the PBDE concentrations prevailing in the sediment during 2005-296
2010. These are likely to reflect decades of inputs, while the mass budget considered inputs over 297
only a limited time period (water years 2005 and 2006). Changes in the use patterns of the 298
various technical PBDE formulations and/or greater persistence of some PBDE congeners could 299
account for some of the discrepancy. The rates of degradation of PBDEs in the environment are 300
not well known. Oram et al. assumed that the degradation rates for PBDEs 47 and 209 were the 301
same, with half-lives of 150 days in water and 578 days in sediment. The PMF results indicate 302
that for PBDEs that have presumably resided in the sediment for several years, only about 13% 303
of the detected moles of BDEs are products of debromination, and much of that debromination 304
may have happened in the atmosphere. Thus the PMF results suggest that the half-lives invoked 305
by Oram et al. are either too fast, or that the products of these degradation processes were not 306
measured in the data set used for PMF analysis (i.e. either degradation processes other than 307
debromination, or complete debromination to diphenyl ether). 308
15
3.4 Debromination and its implications 309
This analysis suggests that congener patterns indicative of debromination of PBDEs are 310
apparent in San Francisco Bay. It is not certain where or how the debromination occurred. It 311
may be the result of photolysis occurring in the gas, dissolved, or suspended sediment phases, 312
microbial debromination under anaerobic conditions, or even debromination by other biota. 313
Debromination products are associated with factors representing 8% of the mass and 13% of the 314
moles of PBDEs in the data matrix, suggesting that PBDEs undergo measurable degradation in 315
the environment. Also, the dibromo congeners PBDE 7, 8, 12, and 15 were detected as 316
debromination products, indicating that debromination has proceeded to an advanced stage. 317
Several other researchers have observed evidence of PBDE debromination in sediments 318
and other environmental compartments. La Guardia et al. (2007) reported PBDEs debromination 319
in sewage sludge and near sewage outfalls. Wei et al. (2012) reported debromination in 320
sediments from Arkansas, but identified the products only by homologue. Salvado et al. (2012) 321
noted decreasing sediment PBDE 209 concentrations and increasing lower molecular weight 322
PBDEs with distance from the probable site of release (Gulf of Lion, Mediterranean Sea). Zhao 323
et al. (2011) found that congeners that were believed to come from photolysis were the most 324
abundant congeners in the sediments of the Daliao River Estuary, China. 325
In a study similar to the present investigation, Zou et al. (2013) used PMF combined with 326
eigenspace projection to investigate PBDE congener patterns in sediments cores from the Great 327
Lakes. Using a data matrix of 10 congeners in 93 samples, they resolved five factors, thought to 328
represent the commercial penta, octa, and deca formulations, and two factors thought to represent 329
debromination products. The first of these was characterized by large contributions from PBDEs 330
66 and 85, while the other was characterized by a high proportion of PBDE 28. Unlike the 331
16
present work, their study did not include congeners 7, 8, 12, 15, and 17, so it is difficult to 332
compare their factors with those resolved in the present study. Nevertheless, it is noteworthy 333
that two studies, one in a freshwater system and one in an estuary, identified two distinct 334
debromination signals in sediment. In the future, we recommend that PBDEs 7, 15, and 17 be 335
routinely monitored, since they appear to be markers for debromination processes. The present 336
analysis did not find an octa signal in San Francisco Bay. PBDE 183, the major congener in the 337
octa formulation, was not included in the data matrix because it was below detection in a 338
majority of samples. However, the maximum contribution of PBDE 183 to the sum of PBDEs 339
was 10%. PBDE 183 comprised more than 2% of the sum of PBDEs in only 11 of 344 samples. 340
In addition, the data matrix did include PBDEs 153, 154, and 155, which are prominent in the 341
octa formulation, yet PMF analysis did not resolve an octa factor. Thus we conclude that the 342
octa formulation is not a major source of PBDEs to San Francisco Bay, possibly due to lower 343
production of octa relative to penta and deca BDE formulations in the Americas (Birnbaum and 344
Staskal, 2004). Also, both the octa and penta BDE formulations have undergone a gradual 345
production bad in California, which was approved in 2003 and fully implemented in 2008. 346
Anaerobic microbial debromination, which we speculate is associated with Factor 3, may 347
have occurred in Bay sediments. Such a process has been shown to debrominate octa mixtures in 348
laboratory microcosms (Lee and He, 2010). It is instructive to consider the similar process of 349
bacterial dechlorination, since in both cases, anaerobic bacteria use the halogenated compound as 350
an electron acceptor. Bacteria capable of dechlorination have been isolated from Bay sediments 351
(Sun et al., 2000; He et al., 2006). Although some researchers have suggested that the threshold 352
concentration for PCB dechlorination is around 40 ppm (Cho et al., 2003), well above the 353
maximum of about 50 ppb reached in Bay sediments, others have shown evidence of PCB 354
17
dechlorination with an enriched culture under substrate concentrations as low as 1 to 5 ppm 355
(Royal et al., 2003; Krumins et al., 2009; Payne et al., 2011). It is also possible that the threshold 356
concentration for PBDE debromination is lower than the threshold for PCBs. Previous studies 357
indicate microbial dechlorination in sewers (Rodenburg et al., 2010; Rodenburg et al., 2012), 358
raising the possibility of microbial debromination in San Francisco Bay area sewers, with 359
debromination products emitted to the Bay via stormwater or treated wastewater outfalls. As 360
noted above, several researchers have seen evidence of PBDE debromination in sewage sludge 361
and near sewage outfalls (La Guardia et al., 2007; Davis et al., 2012). The location of 362
degradation is important. If microbial debromination occurs in Bay sediments, then PBDEs will 363
be less persistent in the long run and will have less tendency to accumulate in sediments. In 364
contrast, if microbial debromination occurs primarily in sewers (i.e., prior to discharge), then 365
both the parent compounds and the debromination products would accumulate in sediments and 366
become problematic in the long term. Based on the increased percent contribution of factor 3 367
from Lower South Bay to South Bay, we hypothesize that the majority of microbial 368
debromination occurs in Bay sediments. Examination of congener ratios in wastewater and 369
treatment plant sludge would aid in confirming this. 370
Regardless of the location of dehalogenation, the results indicate that PBDEs undergo 371
measurable debromination in the environment. We cannot rule out the possibility that 372
debromination leads to the fully debrominated diphenyl ether or to bromophenols (Bendig and 373
Vetter, 2013), which were not measured in this data set. Thus our estimate that about 13% of the 374
moles of PBDEs in the Bay have undergone debromination is a lower bound. This is a relatively 375
large degree of transformation. By comparison, POPs such as PCBs and PCDD/Fs show no 376
evidence of degradation in most aquatic systems. Rodenburg et al. (2010) demonstrate that as 377
18
much as 19% of the PCBs emitted by permitted dischargers in the Delaware River, USA, basin 378
were subject to dehalogenation, but the dechlorination products (primarily PCBs 4 and 19) are 379
barely detectable in Delaware River sediments (Praipipat et al., 2013). These lower chlorinated 380
congeners may be prevented from accumulating in sediments in part due to volatilization, 381
aerobic degradation, or dissolution and advective export. PCBs 4 and 19 have lower octanol-382
water partition coefficients (log Kow = 4.84 for PCB 4 and 5.16 for PCB 19) (Hansen et al., 1999) 383
than PBDE 17 (ranging 5.4 to 6.6) or PBDE 15 (reported at 5.48) (Wania and Dugani, 2003). 384
Thus, dehalogenated PBDE congeners are more likely to accumulate in sediments than the more 385
hydrophilic dehalogenated PCB congeners. The relative toxicity of PBDEs 7, 15, and 17 vs. 386
parent compounds is poorly characterized. If the debromination products have equal or greater 387
toxicity, this would be compounded by the greater environmental mobility and potential 388
exposure to aquatic life associated with lower hydrophobicities (Arnot and Gobas, 2003). For 389
example, PBDE 47 has a greater biota-sediment accumulation factor (BSAF) than PBDE 209 (La 390
Guardia et al., 2012), so debromination of PBDE 209 to PBDE 47 will result in greater 391
bioaccumulation of PBDEs in some organisms. This work has demonstrated that debromination 392
is an important process affecting the fate of PBDE formulations, and that the debromination 393
products accumulate in sediments. Further research is needed to determine the toxic impacts of 394
the debromination products. 395
396
6 ACKNOWLEDGMENTS 397
Sediment PBDE collection and analysis was performed by Applied Marine Sciences, SFEI, the 398
East Bay Municipal Utility District, and Axys Analytical Services, and supported by the 399
19
Regional Monitoring Program for Water Quality in the San Francisco Estuary. BG is supported 400
by a USEPA STAR Fellowship. 401
402
7 REFERENCES 403
Ahn, M.Y., Filley, T.R., Jafvert, C.T., Nies, L., Hua, I., Bezares-Cruz, J., 2006. 404 Photodegradation of decabromodiphenyl ether adsorbed onto clay minerals, metal oxides, 405 and sediment. Environ. Sci. Technol. 40, 215-220. 406
Arnot, J.A., Gobas, F.A.P.C., 2003. A generic QSAR for assessing the bioaccumulation potential 407 of organic chemicals in aquatic food webs. Quant. Struct.-Act. Relat. 22, 1-9. 408
Barabas, N., Goovaerts, P., Adriaens, P., 2004. Modified Polytopic Vector Analysis To Identify 409 and Quantify a Dioxin Dechlorination Signature in Sediments. 2. Application to the Passaic 410 River. Environ. Sci. Technol. 38, 1821-1827. 411
Bedard, D.L., 2003. Polychlorinated biphenyls in aquatic sediments: Environmental fate and 412 outlook for biological treatment. in: Haggblom, M.M., Bossert, I.D. (Eds.). Dehalogenation: 413 Microbial Processes and Environmental Applications. Kluwer Academic Publishers, Boston. 414
Bendig, P., Vetter, W., 2013. UV-Induced Formation of Bromophenols from Polybrominated 415 Diphenyl Ethers. Environ. Sci. Technol. 47, 3665-3670. 416
Birnbaum, L.S., Staskal, D.F., 2004. Brominated flame retardants: Cause for concern? 417 Environmental Health Perspectives 112, 9-17. 418
Brown, S.G., Hafner, H.R., 2003. Exploratory Source Apportionment Of Houston’s Clinton 419 Drive Auto-GC 1998-2001 Data. Texas Commission on Environmental Quality, Petaluma, 420 CA. 421
Buckman, A.H., Wong, C.S., Chow, E.A., Brown, S.B., Solomon, K.R., Fisk, A.T., 2006. 422 Biotransformation of polychlorinated biphenyls (PCBs) and bioformation of hydroxylated 423 PCBs in fish. Aquatic Toxicology 78, 176-185. 424
Bzdusek, P.A., Christensen, E.R., Lee, C.M., Pakdeesusuk, U., Freedman, D.C., 2006a. PCB 425 Congeners and Dechlorination in Sediments of Lake Hartwell, South Carolina, Determined 426 from Cores Collected in 1987 and 1998. Environ. Sci. Technol. 40, 109-119. 427
Bzdusek, P.A., Lu, J., Christensen, E.R., 2006b. PCB Congeners and Dechlorination in Sediment 428 of Sheboygan River, Wisconsin, Determined by Matrix Factorization. Environ. Sci. Technol. 429 40, 120-129. 430
Cho, Y.-C., Sokol, R.C., Frohnhoefer, R.C., Rhee, G.-Y., 2003. Reductive dechlorination of 431 polychlorinated biphenyls: threshold concentration and dechlorination kinetics of individual 432 congeners in Aroclor 1248. Environ. Sci. Technol. 37, 5651-5656. 433
Cloern, J.E., 1996. Phytoplankton bloom dynamics in coastal ecosystems: A review with some 434 general lessons from sustained investigation of San Francisco Bay, California. Reviews of 435 Geophysics 34, 127-168. 436
Conomos, T.J., 1979. Properties and Circulation of San Francisco Bay Waters. in: Conomos, T.J. 437 (Ed.). San Francisco Bay: The Urbanized Estuary. California Academy of Sciences, San 438 Francisco, pp. 47-84. 439
Davis, E.F., Klosterhaus, S.L., Stapleton, H.M., 2012. Measurement of flame retardants and 440 triclosan in municipal sewage sludge and biosolids. Environment International 40, 1-7. 441
20
Davis, J.A., Hetzel, F., Oram, J.J., McKee, L.J., 2007. Polychlorinated biphenyls (PCBs) in San 442 Francisco Bay. Environmental Research 105, 67-86. 443
Deng, D.Y., Guo, J., Sun, G.P., Chen, X.J., Qiu, M.D., Xu, M.Y., 2011. Aerobic debromination 444 of deca-BDE: Isolation and characterization of an indigenous isolate from a PBDE 445 contaminated sediment. International Biodeterioration & Biodegradation 65, 465-469. 446
Ding, C., Chow, W.L., He, J.Z., 2013. Isolation of Acetobacterium sp Strain AG, Which 447 Reductively Debrominates Octa- and Pentabrominated Diphenyl Ether Technical Mixtures. 448 Appl Environ Microbiol 79, 1110-1117. 449
Domingo, J.L., 2012. Polybrominated diphenyl ethers in food and human dietary exposure: A 450 review of the recent scientific literature. Food Chem. Toxicol. 50, 238-249. 451
EPA, U.S., 2007. Method 1614: Brominated Diphenyl Ethers in Water Soil, Sediment and 452 Tissue by HRGC/HRMS. Washington, DC. 453
Fang, L., Huang, J., Yu, G., Wang, L., 2008. Photochemical degradation of six polybrominated 454 diphenyl ether congeners under ultraviolet irradiation in hexane. Chemosphere 71, 258-267. 455
Field, J.A., Sierra-Alvarez, R., 2008. Microbial transformation and degradation of 456 polychlorinated biphenyls. Environ. Pollut. 155, 1-12. 457
Hansen, B.G., Paya-Perez, A.B., Rahman, M., Larsen, B.R., 1999. QSARs for KOW and KOC 458 of PCB congeners: A critical examination of data, assumptions and statistical approaches. 459 Chemosphere 39, 2209-2228. 460
He, J., Robrock, K.R., Alvarez-Cohen, L., 2006. Microbial reductive debromination of 461 polybrominated diphenyl ethers (PBDEs). Environ. Sci. Technol. 40, 4429-4434. 462
Hoenicke, R., Davis, J.A., Gunther, A., Mumley, T.E., Abu-Saba, K., Taberski, K., 2003. 463 Effective application of monitoring information: the case of San Francisco Bay. 464 Environmental Monitoring and Assessment 81, 15-25. 465
Huang, H.L., Zhang, S.Z., Wang, S., Lv, J.T., 2013. In vitro biotransformation of PBDEs by root 466 crude enzyme extracts: Potential role of nitrate reductase (NaR) and glutathione S-transferase 467 (GST) in their debromination. Chemosphere 90, 1885-1892. 468
Imamoglu, I., Li, K., Christensen, E.R., McMullin, J.K., 2004. Sources and Dechlorination of 469 Polychlorinated Biphenyl Congeners in the Sediments of Fox River, Wisconsin. Environ. 470 Sci. Technol. 38, 2574-2583. 471
Klosterhaus, S.L., Stapleton, H.M., La Guardia, M.J., Greig, D.J., 2012. Brominated and 472 chlorinated flame retardants in San Francisco Bay sediments and wildlife. Environment 473 International 47, 56-65. 474
Krumins, V., Park, J.W., Son, E.K., Rodenburg, L.A., Kerkhof, L.J., Haggblom, M.M., Fennell, 475 D.E., 2009. PCB dechlorination enhancement in Anacostia River sediment microcosms. 476 Water Res. 43, 4549-4558. 477
La Guardia, M.J., Hale, R.C., Harvey, E., 2006. Detailed polybrominated diphenyl ether (PBDE) 478 congener composition of the widely used penta-, octa-, and deca-PBDE technical flame-479 retardant mixtures. Environ. Sci. Technol. 40, 6247-6254. 480
La Guardia, M.J., Hale, R.C., Harvey, E., 2007. Evidence of debromination of 481 decabromodiphenyl ether (BDE-209) in biota from a wastewater receiving stream. Environ. 482 Sci. Technol. 41, 6663-6670. 483
La Guardia, M.J., Hale, R.C., Harvey, E., Mainor, T.M., Ciparis, S., 2012. In Situ Accumulation 484 of HBCD, PBDEs, and Several Alternative Flame-Retardants in the Bivalve (Corbicula 485 fluminea) and Gastropod (Elimia proxima). Environ. Sci. Technol. 46, 5798-5805. 486
21
Lee, L.K., Ding, C., Yang, K.L., He, J.Z., 2011. Complete Debromination of Tetra- and Penta-487 Brominated Diphenyl Ethers by a Coculture Consisting of Dehalococcoides and 488 Desulfovibrio Species. Environ. Sci. Technol. 45, 8475-8482. 489
Lee, L.K., He, J., 2010. Reductive Debromination of Polybrominated Diphenyl Ethers by 490 Anaerobic Bacteria from Soils and Sediments. Appl Environ Microbiol 76, 794-802. 491
Lowe, S., Thompson, B., Hoenicke, R., Leatherbarrow, J., Taberski, K., Smith, R., Stevens, D., 492 Jr., 2004. Re-design Process of the San Francisco Estuary Regional Monitoring Program for 493 Trace Substances (RMP) Status & Trends Monitoring Component for Water and Sediment. 494 SFEI, Oakland, CA, p. 86. 495
Magar, V.S., Johnson, G.W., Brenner, R.C., Quensen, J.F., Foote, E.A., Durell, G., Ickes, J.A., 496 McCarthy, C.P., 2005. Long-term Recovery of PCB-Contaminated Sediments at the Lake 497 Hartwell Superfund Site: PCB Dechlorination. 1. End-Member Characteristics. Environ. Sci. 498 Technol. 39, 3538-3547. 499
Mandalakis, M., Besis, A., Stephanou, E.G., 2009. Particle-size distribution and gas/particle 500 partitioning of atmospheric polybrominated diphenyl ethers in urban areas of Greece. 501 Environ. Pollut. 157, 1227-1233. 502
Oram, J.J., McKee, L.J., Werme, C.E., Connor, M.S., Oros, D.R., Grace, R., Rodigari, F., 2008. 503 A mass budget of polybrominated diphenyl ethers in San Francisco Bay, CA. Environment 504 International 34, 1137-1147. 505
Oros, D.R., Hoover, D., Rodigari, F., Crane, D., Sericano, J.L., 2005. Levels and distribution of 506 polybrominated diphenyl ethers in water, surface sediments, and bivalves from the San 507 Francisco Estuary. Environ. Sci. Technol. 39, 33-41. 508
Paatero, P., 2003. User's Guide for Positive Matrix Factorization Programs PMF2 and PMF3. 509 Part 1: Tutorial. 510
Paatero, P., Tapper, U., 1994. Positive Matrix Factorization: a Non-negative Factor Model with 511 Optimal Utilization of Error Estimates of Data Values. Environmetrics 5, 111-126. 512
Payne, R.B., May, H.D., Sowers, K.R., 2011. Enhanced Reductive Dechlorination of 513 Polychlorinated Biphenyl Impacted Sediment by Bioaugmentation with a Dehalorespiring 514 Bacterium. Environ. Sci. Technol. 45, 8772-8779. 515
Praipipat, P., Rodenburg, L.A., Cavallo, G.J., 2013. Source Apportionment of Polychlorinated 516 Biphenyls in the Sediments of the Delaware River. Environ. Sci. Technol. 47, 4277−4283. 517
Robrock, K.R., Korytar, P., Alvarez-Cohen, L., 2008. Pathways for the anaerobic microbial 518 debromination of polybrominated diphenyl ethers. Environ. Sci. Technol. 42, 2845-2852. 519
Rodenburg, L.A., Du, S., Fennell, D.E., Cavallo, G.J., 2010. Evidence for Widespread 520 Dechlorination of Polychlorinated Biphenyls in Groundwater, Landfills, and Wastewater 521 Collection Systems. Environ. Sci. Technol. 44, 7534-7540. 522
Rodenburg, L.A., Du, S.Y., Lui, H., Guo, J., Oseagulu, N., Fennell, D.E., 2012. Evidence for 523 Dechlorination of Polychlorinated Biphenyls and Polychlorinated Dibenzo-p-Dioxins and -524 Furans in Wastewater Collection Systems in the New York Metropolitan Area. Environ. Sci. 525 Technol. 46, 6612-6620. 526
Royal, C.L., Preston, D.R., Sekelsky, A.M., Shreve, G.S., 2003. Reductive dechlorination of 527 polychlorinated biphenyls in landfill leachate. International Biodeterioration & 528 Biodegradation 51, 61 – 66. 529
Salvado, J.A., Grimalt, J.O., Lopez, J.F., de Madron, X.D., Heussner, S., Canals, M., 2012. 530 Transformation of PBDE mixtures during sediment transport and resuspension in marine 531 environments (Gulf of Lion, NW Mediterranean Sea). Environ. Pollut. 168, 87-95. 532
22
Sanchez-Prado, L., Kalafata, K., Risticevic, S., Pawliszyn, J., Lores, M., Llompart, M., 533 Kalogerakis, N., Psillakis, E., 2012. Ice photolysis of 2,2 ',4,4 ',6-pentabromodiphenyl ether 534 (BDE-100): Laboratory investigations using solid phase microextraction. Analytica Chimica 535 Acta 742, 90-96. 536
Sanchez-Prado, L., Lores, M., Llompart, M., Garcia-Jares, C., Bayona, J.M., Cela, R., 2006. 537 Natural sunlight and sun simulator photolysis studies of tetra- to hexa-brominated diphenyl 538 ethers in water using solid-phase microextraction. Journal of Chromatography A 1124, 157-539 166. 540
SFEI, 2012. 2010 Annual Monitoring Results. San Francisco Estuary Institute (SFEI), 541 Richmond, CA. 542
Soonthornnonda, P., Zou, Y.H., Christensen, E.R., Li, A., 2011. PCBs in Great Lakes sediments, 543 determined by positive matrix factorization. Journal of Great Lakes Research 37, 54-63. 544
Stapleton, H.M., Letcher, R.J., Baker, J.E., 2004. Debromination of Polybrominated Diphenyl 545 Ether Congeners BDE 99 and BDE 183 in the Intestinal Tract of the Common Carp 546 (Cyprinus carpio). Environ. Sci. Technol. 38, 1054-1061. 547
Sun, B., Cole, J.R., Sanford, R.A., Tiedje, J.M., 2000. Isolation and characterization of 548 Desulfovibrio dechloracetivorans sp. nov., a marine dechlorinating bacterium growing by 549 coupling the oxidation of acetate to the reductive dechlorination of 2-chlorophenol. Appl. 550 Environ. Microbiol. 66, 2408-2413. 551
Tokarz, J.A., Ahn, M.Y., Leng, J., Filley, T.R., Nies, L., 2008. Reductive debromination of 552 polybrominated diphenyl ethers in anaerobic sediment and a biomimetic system. Environ. 553 Sci. Technol. 42, 1157-1164. 554
United Nations Environment Program, 2009. Stockholm Convention on Persistent Organic 555 Pollutants, Amendments To Annexes A, B And C. United Nations Environment Program, 556 Geneva, Switzerland. 557
Van Aken, B., Correa, P.A., Schnoor, J.L., 2010. Phytoremediation of Polychlorinated 558 Biphenyls: New Trends and Promises. Environ. Sci. Technol. 44, 2767-2776. 559
Wang, S., Zhang, S.Z., Huang, H.L., Lu, A.X., Ping, H., 2012. Debrominated, hydroxylated and 560 methoxylated metabolism in maize (Zea mays L.) exposed to lesser polybrominated diphenyl 561 ethers (PBDEs). Chemosphere 89, 1295-1301. 562
Wania, F., Dugani, C.B., 2003. Assessing the long-range transport potential of polybrominated 563 diphenyl ethers: A comparison of four multimedia models. Environmental Toxicology and 564 Chemistry 22, 1252-1261. 565
Wei, H., Aziz-Schwanbeck, A.C., Zou, Y.H., Corcoran, M.B., Poghosyan, A., Li, A., Rockne, 566 K.J., Christensen, E.R., Sturchio, N.C., 2012. Polybromodiphenyl Ethers and 567 Decabromodiphenyl Ethane in Aquatic Sediments from Southern and Eastern Arkansas, 568 United States. Environ. Sci. Technol. 46, 8017-8024. 569
Wei, H., Zou, Y.H., Li, A., Christensen, E.R., Rockne, K.J., 2013. Photolytic debromination 570 pathway of polybrominated diphenyl ethers in hexane by sunlight. Environ. Pollut. 174, 194-571 200. 572
Zhao, X.F., Zhang, H.J., Ni, Y.W., Lu, X.B., Zhang, X.P., Su, F., Fan, J.F., Guan, D.M., Chen, 573 J.P., 2011. Polybrominated diphenyl ethers in sediments of the Daliao River Estuary, China: 574 Levels, distribution and their influencing factors. Chemosphere 82, 1262-1267. 575
Zou, Y.H., Christensen, E.R., Li, A., 2013. Characteristic pattern analysis of polybromodiphenyl 576 ethers in Great Lakes sediments: a combination of eigenspace projection and positive matrix 577 factorization analysis. Environmetrics 24, 41-50. 578
23
579
580
Figure 1. Map of the San Francisco Bay showing municipal wastewater outfalls.
BD
E7
BD
E8
BD
E12
BD
E15
BD
E17
BD
E28
BD
E35
BD
E37
BD
E47
BD
E49
BD
E51
BD
E66
BD
E71
BD
E85
BD
E99
BD
E10
0
BD
E15
3
BD
E15
4
BD
E15
5
BD
E20
3
BD
E20
6
BD
E20
7
BD
E20
8
BD
E20
9
Frac
tion
of to
tal
0.00
0.05
0.10
0.15
0.20
0.25
0.30B
DE
7
BD
E8
BD
E12
BD
E15
BD
E17
BD
E28
BD
E35
BD
E37
BD
E47
BD
E49
BD
E51
BD
E66
BD
E71
BD
E85
BD
E99
BD
E10
0
BD
E15
3
BD
E15
4
BD
E15
5
BD
E20
3
BD
E20
6
BD
E20
7
BD
E20
8
BD
E20
9
Frac
tion
of to
tal
0.0
0.1
0.2
0.3
0.4
Factor 1 (photolysis)3.1% mass 4.9% moles
BD
E7
BD
E8
BD
E12
BD
E15
BD
E17
BD
E28
BD
E35
BD
E37
BD
E47
BD
E49
BD
E51
BD
E66
BD
E71
BD
E85
BD
E99
BD
E10
0
BD
E15
3
BD
E15
4
BD
E15
5
BD
E20
3
BD
E20
6
BD
E20
7
BD
E20
8
BD
E20
9
Frac
tion
of to
tal
0.00
0.05
0.10
0.15
BD
E7
BD
E8
BD
E12
BD
E15
BD
E17
BD
E28
BD
E35
BD
E37
BD
E47
BD
E49
BD
E51
BD
E66
BD
E71
BD
E85
BD
E99
BD
E10
0
BD
E15
3
BD
E15
4
BD
E15
5
BD
E20
3
BD
E20
6
BD
E20
7
BD
E20
8
BD
E20
9
Frac
tion
of to
tal
0.0
0.1
0.2
0.3
BD
E7
BD
E8
BD
E12
BD
E15
BD
E17
BD
E28
BD
E35
BD
E37
BD
E47
BD
E49
BD
E51
BD
E66
BD
E71
BD
E85
BD
E99
BD
E10
0
BD
E15
3
BD
E15
4
BD
E15
5
BD
E20
3
BD
E20
6
BD
E20
7
BD
E20
8
BD
E20
9
Frac
tion
of to
tal
0.0
0.2
0.4
0.6
0.8
Factor 2 (background) 20% mass21% moles
Factor 3 (microbial debromination) 5.4% mass7.8% moles
Factor 4 (penta-BDE)21% mass26% moles
Factor 5 (deca-BDE)51% mass40% moles
Figure 2. Congener patterns of the five factors resolved by the PMF analysis from the BDE data set.
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
Concentration (ng/g)
!( 0.00 - 0.10!( 0.11 - 0.20!( 0.21 - 0.40!( 0.41 - 0.80!( 0.81 - 1.60!( 1.61 - 3.20!( 3.21 - 6.40!( 6.41 - 12.80
Factor 1 (Microbial or
photochemical debromination)
Factor 2 (PBDE
background)
Factor 3 (Microbial
debromination)Factor 4
(Penta-BDE)
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!(
!(
!(!(!(
!(
!(!(!(!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(!(!(!(!(!( !(!(!(
!(!( !(!( !(
!(!(!(!(!(
!(!(!(!(
!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(!( !(!(!(!(!(!( !(
!(
!(!(!(!(!(
!(!(!(
!(!(
!(!(!(
!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(!(!(!(!( !(!(!(!(!(
!(!(!(!(!(!(!(
!(!(
!(
!(!(!(
!(
!(
!( !(!(
!(
!(
!(!(!(
!(
!(!(!(!(
!(!(!(!(
!(!(!(!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!(
!(!(!( !(
!(
!(
!(!(
!(!(
!(
!(
!(
!(
!(
!(
!(
!(
!(!( !(!(
!(
!(!(
!(!(!(
!(
!(
!(!(
!(
!(
!(
!(
!(
!(!(
!(
!( !(!(!(!( !( !(
!(
!(!(
!(!(
!(!(
!(
!(!(
!(
!(!(!(!(!(
!(
!(!( !(
!( Fraction of total
!( 0.00 - 0.05!( 0.06 - 0.10!( 0.11 - 0.20!( 0.21 - 0.40!( 0.41 - 0.60!( 0.61 - 0.80!( 0.81 - 1.00
Factor 5 (Deca-BDE)
Fraction of total Conc. (ng/g)
Conc. (ng/g)
Conc. (ng/g)
Conc. (ng/g)
Conc. (ng/g)
Fraction of total
Fraction of total
Fraction of total
Fraction of total
Suisun BaySan Pablo Bay
South Bay
Lower South
Bay
2A 2B1A 1B
3A 3B 4A 4B
5A 5B
Photolytic and microbial debromination of brominated diphenyl ether flame retardants in San
Francisco Bay sediment
Lisa A. Rodenburg1*, Qiyun Meng2, Don Yee3, and Ben K. Greenfield3,4
1 Department of Environmental Sciences, Rutgers University, 14 College Farm
Road, New Brunswick, NJ 08901, USA
2School of Public Health, Rutgers Biomedical and Health Sciences, Piscataway, New Jersey 08854, United
States
3San Francisco Estuary Institute, 4911 Central Avenue, Richmond, CA 94804
4Current affiliation: Environmental Health Sciences Division, School of Public Health, University of
California, Berkeley, 50 University Hall #7360, Berkeley, CA 94720-7360
*Corresponding author. Phone 732-932-9800 x 6218, Fax 732-932-8644, email
Supplemental Information 1 Table Supplemental Text: Determination of the correct number of factors 1 Figure
Table S-1. Pearson’s correlation coefficients (r) between the 24 congeners included in the data matrix for PMF analysis.
Determination of the correct number of factors
The number of factors was determined by a weight of evidence approach based on several criteria. First, the relative standard deviation of nine runs of the G matrix using different seed values increased from 1.1% when five factors were requested to 56% when six factors were requested. This is an indication that the PMF2 software cannot find a reproducible (stable) solution when six factors are requested. To determine whether rotation of the five factor solution was necessary, the F peak value was adjusted from -0.3 to 0.3 in 0.1 increments. The resulting Q values changed by less than 0.1%. An F peak value of 0.1 yielded the lowest Q value, but the factors were nearly identical to those generated when F Peak = 0 and the change in the Q value was negligible: Q equaled 3378.40 at F Peak = 0 and 3378.29 when F Peak = 0.1. Furthermore, G-space plots indicated that the five factors were independent of each other (Figure S-1). Thus rotation of the factors was not necessary. In contrast, two of the factors derived when six factors were requested were not independent of each other, as indicated by G-space plots.
This solution provided a good fit to 17 of the 24 congeners, based on an R2 value for the measured versus modeled concentrations of 0.7 or greater, with no more than one outlier discarded per congener. The congeners that were not well described by the five-factor solution were BDE 12 (R2 = 0.57), BDE 35 (0.41), BDE 37 (0.43), BDE 71 (0.44), BDE 85 (0.56), BDE 155 (0.49), and BDE 208 (0.69). BDEs 12, 35, 37, 71, and 155 were below detection limits in between 25 and 59 samples, partially explaining the discrepancy between the measured and modeled concentrations. None of these congeners was crucial to the interpretation of the factors.
BDE 007
BDE 008
BDE 012
BDE 015
BDE 017
BDE 028
BDE 035
BDE 037
BDE 047
BDE 049
BDE 051
BDE 066
BDE 071
BDE 085
BDE 099
BDE 100
BDE 153
BDE 154
BDE 155
BDE 203
BDE 206
BDE 207
BDE 208
BDE 209
BDE 007 0.81 0.33 0.01 0.72 0.55 0.48 0.24 0.52 0.65 0.73 0.51 0.17 0.30 0.45 0.42 0.32 0.57 0.56 0.12 0.37 0.39 0.36 0.19BDE 008 0.60 0.08 0.76 0.59 0.53 0.27 0.44 0.81 0.78 0.51 0.11 0.31 0.34 0.27 0.27 0.45 0.50 0.20 0.48 0.49 0.43 0.26BDE 012 0.37 0.31 0.36 0.44 0.27 0.22 0.53 0.62 0.33 0.01 0.22 0.06 0.22 0.15 0.25 0.28 0.29 0.18 0.19 0.12 0.08BDE 015 0.02 0.36 0.00 0.28 0.19 0.19 0.27 0.35 0.05 0.16 0.04 0.30 0.02 0.17 0.04 0.06 0.08 0.09 0.08 0.03BDE 017 0.78 0.75 0.38 0.68 0.84 0.64 0.64 0.15 0.26 0.48 0.48 0.38 0.63 0.71 0.17 0.54 0.55 0.44 0.34BDE 028 0.61 0.60 0.78 0.79 0.65 0.82 0.14 0.33 0.49 0.64 0.37 0.66 0.68 0.15 0.43 0.43 0.39 0.26BDE 035 0.42 0.65 0.59 0.52 0.50 0.06 0.25 0.36 0.52 0.33 0.61 0.75 0.18 0.55 0.53 0.47 0.49BDE 037 0.56 0.44 0.49 0.73 0.34 0.36 0.32 0.52 0.45 0.49 0.64 0.40 0.25 0.33 0.33 0.11BDE 047 0.68 0.67 0.83 0.20 0.57 0.81 0.92 0.54 0.89 0.73 0.13 0.36 0.39 0.40 0.18BDE 049 0.81 0.80 0.19 0.41 0.52 0.51 0.39 0.64 0.63 0.19 0.48 0.50 0.46 0.25BDE 051 0.72 0.20 0.44 0.49 0.60 0.34 0.63 0.57 0.14 0.28 0.31 0.32 0.12BDE 066 0.22 0.56 0.64 0.76 0.50 0.79 0.70 0.19 0.40 0.46 0.44 0.19BDE 071 0.12 0.21 0.18 0.11 0.20 0.17 0.02 0.10 0.10 0.10 0.08BDE 085 0.83 0.68 0.54 0.76 0.47 0.12 0.22 0.26 0.27 0.08BDE 099 0.81 0.61 0.87 0.56 0.10 0.29 0.33 0.32 0.13BDE 100 0.54 0.93 0.67 0.06 0.20 0.23 0.23 0.08BDE 153 0.65 0.70 0.83 0.34 0.56 0.33 0.18BDE 154 0.78 0.18 0.35 0.42 0.40 0.16BDE 155 0.62 0.46 0.58 0.59 0.22BDE 203 0.38 0.62 0.38 0.35BDE 206 0.92 0.74 0.87BDE 207 0.82 0.73BDE 208 0.40BDE 209
Figure S-1. G-space plots for the five resolved factors