Assessing impacts of unconventional natural gas extraction on microbial communities in headwater stream ecosystems in Northwestern Pennsylvania

Hydraulic fracturing and horizontal drilling have increased dramatically in Pennsylvania Marcellus shale formations, however the potential for major environmental impacts are still incompletely understood. High-throughput sequencing of the 16S rRNA gene was performed to characterize the microbial community structure of water, sediment, bryophyte, and biofilm samples from 26 headwater stream sites in northwestern Pennsylvania with different histories of fracking activity within Marcellus shale formations. Further, we describe the relationship between microbial community structure and environmental parameters measured. Approximately 3.2 million 16S rRNA gene sequences were retrieved from a total of 58 samples. Microbial community analyses showed significant reductions in species richness as well as evenness in sites with Marcellus shale activity. Beta diversity analyses revealed distinct microbial community structure between sites with and without Marcellus shale activity. For example, operational taxonomic units (OTUs) within the Acetobacteracea, Methylocystaceae, Acidobacteriaceae, and Phenylobacterium were greater than three log-fold more abundant in MSA+ sites as compared to MSA− sites. Further, several of these OTUs were strongly negatively correlated with pH and positively correlated with the number of wellpads in a watershed. It should be noted that many of the OTUs enriched in MSA+ sites are putative acidophilic and/or methanotrophic populations. This study revealed apparent shifts in the autochthonous microbial communities and highlighted potential members that could be responding to changing stream conditions as a result of nascent industrial activity in these aquatic ecosystems.

[1]  Karin Ackermann,et al.  Mechanics Of Hydraulic Fracturing , 2016 .

[2]  K. Brubaker,et al.  Marcellus and mercury: Assessing potential impacts of unconventional natural gas extraction on aquatic ecosystems in northwestern Pennsylvania , 2015, Journal of environmental science and health. Part A, Toxic/hazardous substances & environmental engineering.

[3]  Liang Zhao,et al.  Crude Oil Treatment Leads to Shift of Bacterial Communities in Soils from the Deep Active Layer and Upper Permafrost along the China-Russia Crude Oil Pipeline Route , 2014, PloS one.

[4]  R. Jackson,et al.  A critical review of the risks to water resources from unconventional shale gas development and hydraulic fracturing in the United States. , 2014, Environmental science & technology.

[5]  Allen L Robinson,et al.  Air pollutant emissions from the development, production, and processing of Marcellus Shale natural gas , 2014, Journal of the Air & Waste Management Association.

[6]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[7]  S. Launiainen,et al.  Nitrogen, Phosphorus, Carbon, and Suspended Solids Loads from Forest Clear-Cutting and Site Preparation: Long-Term Paired Catchment Studies from Eastern Finland , 2014, AMBIO.

[8]  R. Hammack,et al.  Microbial communities in flowback water impoundments from hydraulic fracturing for recovery of shale gas. , 2013, FEMS microbiology ecology.

[9]  Rob Knight,et al.  EMPeror: a tool for visualizing high-throughput microbial community data , 2013, GigaScience.

[10]  Brian C. Thomas,et al.  Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla , 2013, mBio.

[11]  W. Meng,et al.  Effects of riparian land use on water quality and fish communities in the headwater stream of the Taizi River in China , 2013, Frontiers of Environmental Science & Engineering.

[12]  L. Buňková,et al.  Polyvinyl alcohol biodegradation under denitrifying conditions , 2013 .

[13]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[14]  T. Mincer,et al.  Microbial diversity and methanogenic activity of Antrim Shale formation waters from recently fractured wells , 2013, Front. Microbiol..

[15]  Mark V Brown,et al.  Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. , 2013, Environmental microbiology.

[16]  R. B. Jackson,et al.  Increased stray gas abundance in a subset of drinking water wells near Marcellus shale gas extraction , 2013, Proceedings of the National Academy of Sciences.

[17]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[18]  Sheila M. Olmstead,et al.  Shale gas development impacts on surface water quality in Pennsylvania , 2013, Proceedings of the National Academy of Sciences.

[19]  D. Zavala-Araiza,et al.  Regional air quality impacts of increased natural gas production and use in Texas. , 2013, Environmental science & technology.

[20]  N. Vidic,et al.  Spatial and temporal correlation of water quality parameters of produced waters from devonian-age shale following hydraulic fracturing. , 2013, Environmental science & technology.

[21]  Reg.  Investigation of Ground - Water Contamination near Pavillion, Wyoming: Workgroup Meeting, November 30, 2011 , 2013 .

[22]  S. Grasby,et al.  The Paint Pots, Kootenay National Park, Canada — a natural acid spring analogue for Mars1,2 , 2013 .

[23]  Frank Spellman,et al.  Chemicals Used in Hydraulic Fracturing , 2012 .

[24]  P. Dunfield,et al.  Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing , 2012, Front. Microbio..

[25]  R. Jackson,et al.  Geochemical evidence for possible natural migration of Marcellus Formation brine to shallow aquifers in Pennsylvania , 2012, Proceedings of the National Academy of Sciences.

[26]  S. Wondzell,et al.  Headwater stream temperature: Interpreting response after logging, with and without riparian buffers, Washington, USA , 2012 .

[27]  K. Kidd,et al.  Aquatic and terrestrial organic matter in the diet of stream consumers: implications for mercury bioaccumulation. , 2012, Ecological applications : a publication of the Ecological Society of America.

[28]  Phenylobacterium muchangponense sp. nov., isolated from beach soil, and emended description of the genus Phenylobacterium. , 2012, International journal of systematic and evolutionary microbiology.

[29]  P. Drohan,et al.  Early Trends in Landcover Change and Forest Fragmentation Due to Shale-Gas Development in Pennsylvania: A Potential Outcome for the Northcentral Appalachians , 2012, Environmental Management.

[30]  J. Webber.  Water Quality Condition Assessment of Streams in National Parks of the Mid-Atlantic USA Integrating Physical, Chemical, and Biological Datasets , 2012 .

[31]  H. Laudon,et al.  Effects of forestry operations on dissolved organic carbon concentrations and export in boreal first‐order streams , 2012 .

[32]  E. K. Hall,et al.  Effects of Resource Chemistry on the Composition and Function of Stream Hyporheic Biofilms , 2012, Front. Microbio..

[33]  Julie M. Fagan,et al.  Chemicals Used in Hydraulic Fracturing , 2012 .

[34]  Impaired Leaf Litter Processing in Acidified Streams , 2012, Microbial Ecology.

[35]  B. Johnson,et al.  Rapid expansion of natural gas development poses a threat to surface waters , 2011 .

[36]  R. Davies.  Methane contamination of drinking water caused by hydraulic fracturing remains unproven , 2011, Proceedings of the National Academy of Sciences.

[37]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[38]  Christopher G. Struchtemeyer,et al.  Influence of the Drilling Mud Formulation Process on the Bacterial Communities in Thermogenic Natural Gas Wells of the Barnett Shale , 2011, Applied and Environmental Microbiology.

[39]  Donald E. Weller,et al.  Anthropogenic disturbance and streams: land use and land‐use change affect stream ecosystems via multiple pathways , 2011 .

[40]  P. D’haeseleer,et al.  Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria , 2010, Science.

[41]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[42]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[43]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[44]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[45]  P. Kaufmann,et al.  Protecting sediment-sensitive aquatic species in mountain streams through the application of biologically based streambed sediment criteria , 2010, Journal of the North American Benthological Society.

[46]  E. F. Benfield,et al.  Variation in ecosystem function in Appalachian streams along an acidity gradient. , 2009, Ecological applications : a publication of the Ecological Society of America.

[47]  D. Wagner,et al.  Diversity of Aerobic Methanotrophic Bacteria in a Permafrost Active Layer Soil of the Lena Delta, Siberia , 2008, Microbial Ecology.

[48]  J. Daniel Arthur,et al.  AN OVERVIEW OF MODERN SHALE GAS DEVELOPMENT IN THE UNITED STATES , 2008 .

[49]  Noah Fierer,et al.  Environmental controls on the landscape-scale biogeography of stream bacterial communities. , 2007, Ecology.

[50]  Mary C. Freeman,et al.  Hydrologic Connectivity and the Contribution of Stream Headwaters to Ecological Integrity at Regional Scales 1 , 2007 .

[51]  Robert J. Naiman,et al.  Ecological Linkages Between Headwaters and Downstream Ecosystems: Transport of Organic Matter, Invertebrates, and Wood Down Headwater Channels 1 , 2007 .

[52]  Gregory E Schwarz,et al.  The Role of Headwater Streams in Downstream Water Quality1 , 2007, Journal of the American Water Resources Association.

[53]  D. Strayer,et al.  The Contribution of Headwater Streams to Biodiversity in River Networks 1 , 2007 .

[54]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[55]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[56]  F. Lingens,et al.  The Genus Phenylobacterium , 2006 .

[57]  J. Silverstein,et al.  Denitrification Potential in Stream Sediments Impacted by Acid Mine Drainage: Effects of pH, Various Electron Donors, and Iron , 2006, Microbial Ecology.

[58]  A. Mills,et al.  Changes in water and sediment bacterial community structure in a lake receiving acid mine drainage , 1983, Microbial Ecology.

[59]  J. Hammarstrom,et al.  Acid-rock drainage at Skytop, Centre County, Pennsylvania, 2004 , 2005 .

[60]  A. Covich,et al.  Relative Importance of Bacteria and Fungi in a Tropical Headwater Stream: Leaf Decomposition and Invertebrate Feeding Preference , 2005, Microbial Ecology.

[61]  Olivier Dangles,et al.  Impacts of stream acidification on litter breakdown: implications for assessing ecosystem functioning , 2004 .

[62]  J. Elwood,et al.  Relationships between stream acidity and bacteria, macroinvertebrates, and fish: a comparison of north temperate and south temperate mountain streams, USA , 1992, Hydrobiologia.

[63]  D. McKnight,et al.  The ecological effect of acid conditions and precipitation of hydrous metal oxides in a Rocky Mountain stream , 1984, Hydrobiologia.

[64]  S. Fazi,et al.  Bacterial uptake of DOM released from P-limited phytoplankton. , 2003, FEMS microbiology ecology.

[65]  Jennifer L. Tank,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Ecosystem metabolism controls nitrogen uptake in streams in Grand Teton National , 2022 .

[66]  V. Gulis,et al.  Leaf litter decomposition and microbial activity in nutrient‐enriched and unaltered reaches of a headwater stream , 2003 .

[67]  S. Hamilton,et al.  A Cross-System Comparison of Bacterial and Fungal Biomass in Detritus Pools of Headwater Streams , 2002, Microbial Ecology.

[68]  S. Hamilton,et al.  Control of Nitrogen Export from Watersheds by Headwater Streams , 2001, Science.

[69]  R. Amann,et al.  Combined Use of 16S Ribosomal DNA and 16S rRNA To Study the Bacterial Community of Polychlorinated Biphenyl-Polluted Soil , 2001, Applied and Environmental Microbiology.

[70]  L. Leff,et al.  Bacterial Populations in an Anthropogenically Disturbed Stream: Comparison of Different Seasons , 1999, Microbial Ecology.

[71]  B. K. Ellis,et al.  The role of micro‐organisms in the ecological connectivity of running waters , 1998 .

[72]  Sigmund Jensen,et al.  Microbial Community Changes in a Perturbed Agricultural Soil Investigated by Molecular and Physiological Approaches , 1998, Applied and Environmental Microbiology.

[73]  L. Leff,et al.  The Response of Three Bacterial Populations to Pollution in a Stream , 1997, Microbial Ecology.

[74]  L. A. Smock,et al.  Spatial and temporal variation of microbial respiration rates in a blackwater stream , 1996 .

[75]  C. J. Gagen,et al.  Episodic acidification of small streams in the northeastern united states: Effects on fish populations , 1996 .

[76]  Bernard W. Sweeney,et al.  Streamside Forests and the Physical, Chemical, and Trophic Characteristics of Piedmont Streams in Eastern North America , 1992 .

[77]  K. Karbaum,et al.  Acetobacter methanolicus sp. nov., an acidophilic facultatively methylotrophic bacterium , 1986 .

[78]  Cathy M. Tate,et al.  The Effects of Watershed Disturbance on Dissolved Organic Carbon Dynamics of a Stream , 1983 .

[79]  P. Sollins,et al.  Nitrogen and carbon solution chemistry of an old growth coniferous forest watershed before and after cutting , 1981 .