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Lawrence Berkeley National Laboratory Recent Work Title Bacterial Biomarkers of Marcellus Shale Activity in Pennsylvania. Permalink https://escholarship.org/uc/item/40b5p10v Journal Frontiers in microbiology, 9(AUG) ISSN 1664-302X Authors Chen See, Jeremy R Ulrich, Nikea Nwanosike, Hephzibah et al. Publication Date 2018 DOI 10.3389/fmicb.2018.01697 Peer reviewed eScholarship.org Powered by the California Digital Library University of California fmicb-09-01697 July 30, 2018 Time: 16:56 # 1 ORIGINAL RESEARCH published: 02 August 2018 doi: 10.3389/fmicb.2018.01697 Bacterial Biomarkers of Marcellus Shale Activity in Pennsylvania Jeremy R. Chen See1, Nikea Ulrich1, Hephzibah Nwanosike1, Christopher J. McLimans1, Vasily Tokarev1, Justin R. Wright1, Maria F. Campa2, Christopher J. Grant1, Terry C. Hazen2,3,4, Jonathan M. Niles5, Daniel Ressler6 and Regina Lamendella1* 1 Department of Biology, Juniata College, Huntingdon, PA, United States, 2 The Bredesen Center, The University of Tennessee, Knoxville, Knoxville, TN, United States, 3 Department of Civil and Environmental Engineering, The University of Tennessee, Knoxville, Knoxville, TN, United States, 4 Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, United States, 5 Freshwater Research Initiative, Susquehanna University, Selinsgrove, PA, United States, 6 Department of Earth and Environmental Sciences, Susquehanna University, Selinsgrove, PA, United States Unconventional oil and gas (UOG) extraction, also known as hydraulic fracturing, is becoming more prevalent with the increasing use and demand for natural gas; however, the full extent of its environmental impacts is still unknown. Here we measured physicochemical properties and bacterial community composition of sediment samples Edited by: taken from twenty-eight streams within the Marcellus shale formation in northeastern James Cotner, Pennsylvania differentially impacted by hydraulic fracturing activities. Fourteen of the University of Minnesota Twin Cities, streams were classified as UOGC, and thirteen were classified as UOG− based on the United States presence of UOG extraction in their respective watersheds. One stream was located in Reviewed by: Jennifer F. Biddle, a watershed that previously had UOG extraction activities but was recently abandoned. University of Delaware, United States We utilized high-throughput sequencing of the 16S rRNA gene to infer differences in Casey Michael Godwin, C − University of Michigan, United States sediment aquatic bacterial community structure between UOG and UOG streams, *Correspondence: as well as correlate bacterial community structure to physicochemical water parameters. Regina Lamendella Although overall alpha and beta diversity differences were not observed, there were a [email protected] plethora of significantly enriched operational taxonomic units (OTUs) within UOGC and − Specialty section: UOG samples. Our biomarker analysis revealed many of the bacterial taxa enriched This article was submitted to in UOGC streams can live in saline conditions, such as Rubrobacteraceae. In addition, Aquatic Microbiology, several bacterial taxa capable of hydrocarbon degradation were also enriched in UOGC a section of the journal Frontiers in Microbiology samples, including Oceanospirillaceae. Methanotrophic taxa, such as Methylococcales, Received: 06 March 2018 were significantly enriched as well. Several taxa that were identified as enriched in these Accepted: 09 July 2018 samples were enriched in samples taken from different streams in 2014; moreover, Published: 02 August 2018 partial least squares discriminant analysis (PLS-DA) revealed clustering between streams Citation: Chen See JR, Ulrich N, Nwanosike H, from the different studies based on the presence of hydraulic fracturing along the McLimans CJ, Tokarev V, Wright JR, second axis. This study revealed significant differences between bacterial assemblages Campa MF, Grant CJ, Hazen TC, within stream sediments of UOGC and UOG− streams and identified several potential Niles JM, Ressler D and Lamendella R (2018) Bacterial Biomarkers biomarkers for evaluating and monitoring the response of autochthonous bacterial of Marcellus Shale Activity communities to potential hydraulic fracturing impacts. in Pennsylvania. Front. Microbiol. 9:1697. Keywords: hydraulic fracturing, fracking, Marcellus shale, 16S rRNA gene sequencing, microbial communities, doi: 10.3389/fmicb.2018.01697 biomarkers, halophilic, hydrocarbons Frontiers in Microbiology| www.frontiersin.org 1 August 2018| Volume 9| Article 1697 fmicb-09-01697 July 30, 2018 Time: 16:56 # 2 Chen See et al. Biomarkers of Marcellus Shale Activity INTRODUCTION indicators of stream quality, as microbes can quickly respond to disturbances (Hunt and Ward, 2015). In addition, microbes Over the past several years, the rapid increased use of natural are the most abundant organisms in aquatic communities, by gas in the United States (Lieskovsky et al., 2014; Laurenzi et al., concentration and often even by biomass (Hunt and Ward, 2015). 2016; U.S. EIA, 2017a) has been driven by horizontal drilling and As a result, they play an important role in cycling energy and hydraulic fracturing (Brittingham et al., 2014; Jackson et al., 2014; nutrients. Microbial communities have been found to change Burden et al., 2016). During hydraulic fracturing, a mixture of in response to anthropogenic activities, such as agriculture, water, proppants, and chemicals is injected into a rock formation industry, and mining (Wassel and Mills, 1983; Essahale et al., to create fractures, allowing natural gas to flow to the surface 2010; Stutter and Cains, 2017). (Jackson et al., 2014; Silva et al., 2014). Hydraulic fracturing will Recent work has found streams near hydraulic fracturing become more prevalent as the use and demand for natural gas experience drastic shifts in certain bacterial assemblages increases. By 2050, the use of natural gas is predicted to increase (Acetobacteraceae, Methylocystaceae, and Phenylobacterium) more than any other fuel source in the United States (U.S. EIA, and had lower observed bacterial diversity (Trexler et al., 2014). 2017a). In the EIA’s reference case, natural gas consumption However, a study done in the Fayetteville shale formation increases by 6.4 quadrillion BTUs to 32.27 quadrillion BTUs from did not find any significant difference in alpha diversity 2015 to 2050 in the United States (U.S. EIA, 2017a), and by 90.8 based on proximity to hydraulic fracturing, but it too noted quadrillion BTUs from 2014 to 2050 to 218.2 quadrillion BTUs an increased abundance of specific taxa (Microcystis and globally (U.S. EIA, 2017b). In the United States, the Marcellus Synechoccophycideae) in streams near hydraulic fracturing and Utica formations are predicted to be the primary drivers of operations (Johnson et al., 2017). Furthermore, that study noted this growth (U.S. EIA, 2017a). little work has been done on evaluating the impact of hydraulic Technological advances in natural gas extraction have far fracturing on streams. This is especially surprising considering outpaced our ability to evaluate the potential environmental their importance and sensitivity to environmental disturbances. impacts of this process. Recent research has indicated possible More recently, specific bacteria, including the aptly named contamination of water resources by nascent hydraulic fracturing Frackibacter, have been found to be associated with hydraulic activities (Rahm and Riha, 2012; Jackson et al., 2013; DiGiulio fracturing (Daly et al., 2016; Mouser et al., 2016). Here we utilized and Jackson, 2016). Hydraulic fracturing produces a large amount bacterial community profiling to address the aquatic bacterial of saline wastewater (Veil et al., 2004; Cluff et al., 2014; Silva response (n = 31 streams) to potential hydraulic fracturing et al., 2014); wastewater can enter nearby groundwater or surface inputs in Pennsylvania, which is experiencing the most rapid water via faulty well casings, leaks in holding ponds, or spills development in UOG in the United States (U.S. EIA, 2016). We (Vidic et al., 2013). This could be especially problematic as hypothesized that the alpha and beta diversity of UOGC and high salinities can inhibit the biodegradation of potentially UOG− streams would differ significantly and certain OTUs and harmful chemicals in hydraulic fracturing fluid (Kekacs et al., pathways would be enriched based on proximity to hydraulic 2015), several of which have been found in produced water fracturing. High-throughput sequencing of the 16S rRNA gene (Burden et al., 2016). Furthermore, there have been over 4,000 and random forest modeling enabled the identification of several violations of environmental health and safety regulations for bacterial taxa that were enriched and predictive of UOG status of hydraulic fracturing operations in Pennsylvania since 2009 (PA a given stream. The data generated in this study can potentially DEP, 2017a). Additionally, changes in land use can also impact be used and combined with future aquatic microbial ecology adjacent streams, as each well pad needs between 1.2 and 2.7 studies to generate more comprehensive spatial and temporal acres of land on average (Brittingham et al., 2014). Increased biomarkers of UOG activity. overland flow due to forest disturbance has been found to affect water quality (Schelker et al., 2012; Palviainen et al., 2014). Undoubtedly then, hydraulic fracturing has the potential to affect MATERIALS AND METHODS nearby water resources. This issue is especially
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