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Sci Total Environ
2023 Jul 01;880:163160. doi: 10.1016/j.scitotenv.2023.163160.
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Energy-related wastewater contamination alters microbial communities of sediment, water, and amphibian skin.
Tornabene BJ
,
Smalling KL
,
Givens CE
,
Oja EB
,
Hossack BR
.
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To inform responsible energy development, it is important to understand the ecological effects of contamination events. Wastewaters, a common byproduct of oil and gas extraction, often contain high concentrations of sodium chloride (NaCl) and heavy metals (e.g., strontium and vanadium). These constituents can negatively affect aquatic organisms, but there is scarce information for how wastewaters influence potentially distinct microbiomes in wetland ecosystems. Additionally, few studies have concomitantly investigated effects of wastewaters on the habitat (water and sediment) and skin microbiomes of amphibians or relationships among these microbial communities. We sampled microbiomes of water, sediment, and skin of four larval amphibian species across a gradient of chloride contamination (0.04-17,500 mg/L Cl) in the Prairie Pothole Region of North America. We detected 3129 genetic phylotypes and 68 % of those phylotypes were shared among the three sample types. The most common shared phylotypes were Proteobacteria, Firmicutes, and Bacteroidetes. Salinity of wastewaters increased dissimilarity within all three microbial communities, but not the diversity or richness of water and skin microbial communities. Strontium was associated with lower diversity and richness of sediment microbial communities, but not those of water or amphibian skin, likely because metal deposition occurs in sediment when wetlands dry. Based on Bray Curtis distance matrices, sediment microbiomes were similar to those of water, but neither had substantial overlap with amphibian microbiomes. Species identity was the strongest predictor of amphibian microbiomes; frog microbiomes were similar but differed from that of the salamander, whose microbiome had the lowest richness and diversity. Understanding how effects of wastewaters on the dissimilarity, richness, and diversity of microbial communities also influence the ecosystem function of communities will be an important next step. However, our study provides novel insight into the characteristics of, and associations among, different wetland microbial communities and effects of wastewaters from energy production.
Fig. 1. Study area including sites within US Fish and Wildlife (USFWS) Waterfowl Production Areas and private property in Montana and North Dakota within the Williston Basin and Prairie Pothole Region where we collected water, sediment, and larval amphibian skin microbiome samples. NWR = National Wildlife Refuge. See Table S1 for additional attributes. Baselayer sources: Esri, HERE, Garmin, SafeGraph, FAO, METI/NASA, USGS, EPA, NOAA, State of North Dakota.
Fig. 2. Percent (%) sequence reads per microbial phylum and site for sediment (A) and water samples (B) collected at 27 and 28 wetland sites in the Prairie Pothole Region. Sites are ordered from lowest (left) to highest (right) salinity on the x-axis (refer to Table 1). Note that one sediment sample (from site '264-Z') was not included in analyses because it did not pass quality assurance (missing from panel A, asterisk [*] in panel B).
Fig. 3. Percent (%) sequence reads per microbial phylotype and amphibian species for skin samples collected at 18 wetlands in the Prairie Pothole Region. For species, AMMA = barred tiger salamander (Ambystoma mavortium), LIPI = northern leopard frogs (Lithobates pipiens), LISY = wood frogs (Lithobates sylvaticus), and PSMA = boreal chorus frogs (Pseudacris maculata).
Fig. 4. Ordination plot of the first two of a four-dimensional non-metric multidimensional scaling plot (with 95 % confidence ellipses) of Bray Curtis microbial community dissimilarities from samples obtained from water, sediment, and amphibian skin at up to 28 wetland sites in the Prairie Pothole Region (stress value = 0.12). The black circles mark the centroids of each ellipse.
Fig. 5. Ordination plot of the first two of a three-dimensional non-metric multidimensional scaling plots of Bray Curtis dissimilarities of microbial communities in samples obtained from sediment (panel A, stress value = 0.07) and water (panel B, stress value = 0.06) from up to 28 wetlands in the Prairie Pothole Region. Vectors drawn on the plots represent environmental variables and constituents of wastewaters measured at each wetland, including concentrations of vanadium, strontium, and chloride, wetland area, vegetation cover, and percent shallows (proportion of wetland ≤ 0.5 m deep).
Fig. 6. Ordination plot of the first two of a four-dimensional non-metric multidimensional scaling plots of Bray Curtis dissimilarities of skin microbial communities of larval amphibians from 18 wetlands across the Prairie Pothole Region (stress value = 0.12). Four species of amphibians were sampled, including barred tiger salamanders (Ambystoma mavortium; AMMA), northern leopard frogs (Lithobates pipiens; LIPI), wood frogs (Lithobates sylvaticus; LISY), and boreal chorus frogs (Pseudacris maculata; PSMA). In panel B, vectors drawn on the plots represent environmental variables measured at each wetland site, including concentrations of vanadium, strontium, and chloride, and wetland area, vegetation cover, and percent shallows. The small filled circles mark the centroids of each species ellipse in panel B.
Figure S1. Scree plots visualizing change in non-metric multidimensional scaling stress values
with increasing dimensions in NMDS analyses of Bray Curtis distance matrices from (A) all
sample types and separately for (B) water, (C) sediment, and (D) amphibian skin microbiomes.
Figure S2. Percent (%) sequence reads per microbial phyla and amphibian species for skin
samples collected at 18 wetland sites in the Prairie Pothole Region. For species, AMMA =
Barred Tiger Salamander (Ambystoma mavortium), LIPI = Northern Leopard Frogs (Lithobates
pipiens), LISY = Wood Frogs (Lithobates sylvaticus), and PSMA = Boreal chorus frogs
(Pseudacris maculata).
Figure S3. Heatmap comparing relative abundance of selected phylotypes from amphibian skin
across sites, ordered from lowest (left) to highest (right) salinity (based on chloride
concentrations) on x-axis, collected from 18 wetlands in the Prairie Pothole Region. Only the top
21 phylotypes (observed in > 50% of samples) were included.