Natural Bacterial Communities Serve as Quantitative Geochemical Biosensors

Author:

Smith Mark B.1,Rocha Andrea M.2,Smillie Chris S.3,Olesen Scott W.4,Paradis Charles5,Wu Liyou6,Campbell James H.27,Fortney Julian L.8,Mehlhorn Tonia L.9,Lowe Kenneth A.9,Earles Jennifer E.9,Phillips Jana9,Techtmann Steve M.8ORCID,Joyner Dominique C.8,Elias Dwayne A.2,Bailey Kathryn L.2,Hurt Richard A.2,Preheim Sarah P.4,Sanders Matthew C.4,Yang Joy3,Mueller Marcella A.9,Brooks Scott9,Watson David B.9,Zhang Ping6,He Zhili6,Dubinsky Eric A.10,Adams Paul D.1011,Arkin Adam P.1011,Fields Matthew W.12,Zhou Jizhong6,Alm Eric J.134,Hazen Terry C.25813ORCID

Affiliation:

1. Microbiology Graduate Program, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

2. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA

3. Computational and Systems Biology Initiative, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

4. Biological Engineering Department, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

5. Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee, USA

6. Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA

7. Department of Natural Sciences, Northwest Missouri State University, Maryville, Missouri, USA

8. Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA

9. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA

10. Lawrence Berkeley National Laboratory, Berkeley, California, USA

11. Department of Bioengineering, University of California, Berkeley, California, USA

12. Department of Microbiology & Immunology, Montana State University, Bozeman, Montana, USA

13. Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA

Abstract

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. IMPORTANCE 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.

Publisher

American Society for Microbiology

Subject

Virology,Microbiology

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