title: Natural bacterial communities serve as quantitative geochemical biosensors.
abstract: Biological sensors can be engineered to measure a wide range of environmental conditions. Here we show that statistical analysis of DNA from natural microbial communities can be used to accurately identify environmental contaminants, including uranium and nitrate at a nuclear waste site. In addition to contamination, sequence data from the 16S rRNA gene alone can quantitatively predict a rich catalogue of 26 geochemical features collected from 93 wells with highly differing geochemistry characteristics. We extend this approach to identify sites contaminated with hydrocarbons from the Deepwater Horizon oil spill, finding that altered bacterial communities encode a memory of prior contamination, even after the contaminants themselves have been fully degraded. We show that the bacterial strains that are most useful for detecting oil and uranium are known to interact with these substrates, indicating that this statistical approach uncovers ecologically meaningful interactions consistent with previous experimental observations. Future efforts should focus on evaluating the geographical generalizability of these associations. Taken as a whole, these results indicate that ubiquitous, natural bacterial communities can be used as in situ environmental sensors that respond to and capture perturbations caused by human impacts. These in situ biosensors rely on environmental selection rather than directed engineering, and so this approach could be rapidly deployed and scaled as sequencing technology continues to become faster, simpler, and less expensive.
  
  
  OBJECTIVE
  Here we show that DNA from natural bacterial communities can be used as a quantitative biosensor to accurately distinguish unpolluted sites from those contaminated with uranium, nitrate, or oil. These results indicate that bacterial communities can be used as environmental sensors that respond to and capture perturbations caused by human impacts.
authors.affiliation: Microbiology Graduate Program, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Mark B
authors.initials: MB
authors.lastname: Smith
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Andrea M
authors.initials: AM
authors.lastname: Rocha
authors.affiliation: Computational and Systems Biology Initiative, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Chris S
authors.initials: CS
authors.lastname: Smillie
authors.affiliation: Biological Engineering Department, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Scott W
authors.initials: SW
authors.lastname: Olesen
authors.affiliation: Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee, USA.
authors.forename: Charles
authors.initials: C
authors.lastname: Paradis
authors.affiliation: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Liyou
authors.initials: L
authors.lastname: Wu
authors.forename: James H
authors.initials: JH
authors.lastname: Campbell
authors.affiliation: Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA.
authors.forename: Julian L
authors.initials: JL
authors.lastname: Fortney
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Tonia L
authors.initials: TL
authors.lastname: Mehlhorn
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Kenneth A
authors.initials: KA
authors.lastname: Lowe
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Jennifer E
authors.initials: JE
authors.lastname: Earles
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Jana
authors.initials: J
authors.lastname: Phillips
authors.affiliation: Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA.
authors.forename: Steve M
authors.identifier: http://orcid.org/0000-0002-8702-9329
authors.initials: SM
authors.lastname: Techtmann
authors.affiliation: Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA.
authors.forename: Dominique C
authors.initials: DC
authors.lastname: Joyner
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Dwayne A
authors.initials: DA
authors.lastname: Elias
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Kathryn L
authors.initials: KL
authors.lastname: Bailey
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Richard A
authors.initials: RA
authors.lastname: Hurt
authors.affiliation: Biological Engineering Department, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Sarah P
authors.initials: SP
authors.lastname: Preheim
authors.affiliation: Biological Engineering Department, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Matthew C
authors.initials: MC
authors.lastname: Sanders
authors.affiliation: Computational and Systems Biology Initiative, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
authors.forename: Joy
authors.initials: J
authors.lastname: Yang
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Marcella A
authors.initials: MA
authors.lastname: Mueller
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: Scott
authors.initials: S
authors.lastname: Brooks
authors.affiliation: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.
authors.forename: David B
authors.initials: DB
authors.lastname: Watson
authors.affiliation: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Ping
authors.initials: P
authors.lastname: Zhang
authors.affiliation: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Zhili
authors.initials: Z
authors.lastname: He
authors.affiliation: Lawrence Berkeley National Laboratory, Berkeley, California, USA.
authors.forename: Eric A
authors.initials: EA
authors.lastname: Dubinsky
authors.forename: Paul D
authors.initials: PD
authors.lastname: Adams
authors.forename: Adam P
authors.initials: AP
authors.lastname: Arkin
authors.affiliation: Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA.
authors.forename: Matthew W
authors.initials: MW
authors.lastname: Fields
authors.affiliation: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Jizhong
authors.initials: J
authors.lastname: Zhou
authors.forename: Eric J
authors.initials: EJ
authors.lastname: Alm
authors.affiliation: tchazen@utk.edu.
authors.forename: Terry C
authors.identifier: http://orcid.org/0000-0002-2536-9993
authors.initials: TC
authors.lastname: Hazen
mesh_terms: D001419:Bacteria / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism*; D015374:Biosensing Techniques; D004269:DNA, Bacterial / Q000032:analysis; D004275:DNA, Ribosomal / Q000235:genetics; D017753:Ecosystem; D020459:Genes, rRNA; D060587:Groundwater / Q000737:chemistry / Q000382:microbiology*; D006838:Hydrocarbons / Q000032:analysis; D059013:Microbial Consortia / Q000235:genetics; D009566:Nitrates / Q000032:analysis; D059392:Petroleum Pollution / Q000032:analysis*; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D014501:Uranium / Q000032:analysis; D014873:Water Pollutants / Q000032:analysis*; D014878:Water Pollution, Radioactive / Q000032:analysis
chemical_list: D004269:DNA, Bacterial; D004275:DNA, Ribosomal; D006838:Hydrocarbons; D009566:Nitrates; D012336:RNA, Ribosomal, 16S; D014873:Water Pollutants; D014501:Uranium