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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, andmore » so this approach could be rapidly deployed and scaled as sequencing technology continues to become faster, simpler, and less expensive. 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.« less

Authors:
 [1];  [2];  [1];  [1];  [3];  [4];  [5];  [3];  [2];  [2];  [2];  [2]; ORCiD logo [3];  [3];  [2];  [2];  [1];  [1];  [1];  [1] more »;  [2];  [2];  [2];  [4];  [4];  [6];  [6];  [6];  [6];  [4];  [1]; ORCiD logo [2] « less
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  2. Oak Ridge National Laboratory, Oak Ridge, TN (United States). Environmental Sciences Division.
  3. Univ. of Knoxville, Knoxville, TN (United States)
  4. Univ. of Oklahoma, Norman, OK (United States)
  5. Oak Ridge National Laboratory, Oak Ridge, TN (United States), Biosciences Division.
  6. Lawrence Berkeley National Laboratory, Berkeley, California, (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1215642
Alternate Identifier(s):
OSTI ID: 1265499
Grant/Contract Number:
AC02-05CH11231; AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; ENIGMA

Citation Formats

Smith, Mark B., Rocha, Andrea M., Smillie, Chris S., Olesen, Scott W., Paradis, Charles, Wu, Liyou, Campbell, James H., Fortney, Julian L., Mehlhorn, Tonia L., Lowe, Kenneth A., Earles, Jennifer E., Phillips, Jana, Techtmann, Steve M., Joyner, Dominique C., Elias, Dwayne A., Bailey, Kathryn L., Hurt, Richard A., Preheim, Sarah P., Sanders, Matthew C., Yang, Joy, Mueller, Marcella A., Brooks, Scott, Watson, David B., Zhang, Ping, He, Zhili, Dubinsky, Eric A., Adams, Paul D., Arkin, Adam P., Fields, Matthew W., Zhou, Jizhong, Alm, Eric J., and Hazen, Terry C. Natural bacterial communities serve as quantitative geochemical biosensors. United States: N. p., 2015. Web. doi:10.1128/mBio.00326-15.
Smith, Mark B., Rocha, Andrea M., Smillie, Chris S., Olesen, Scott W., Paradis, Charles, Wu, Liyou, Campbell, James H., Fortney, Julian L., Mehlhorn, Tonia L., Lowe, Kenneth A., Earles, Jennifer E., Phillips, Jana, Techtmann, Steve M., Joyner, Dominique C., Elias, Dwayne A., Bailey, Kathryn L., Hurt, Richard A., Preheim, Sarah P., Sanders, Matthew C., Yang, Joy, Mueller, Marcella A., Brooks, Scott, Watson, David B., Zhang, Ping, He, Zhili, Dubinsky, Eric A., Adams, Paul D., Arkin, Adam P., Fields, Matthew W., Zhou, Jizhong, Alm, Eric J., & Hazen, Terry C. Natural bacterial communities serve as quantitative geochemical biosensors. United States. doi:10.1128/mBio.00326-15.
Smith, Mark B., Rocha, Andrea M., Smillie, Chris S., Olesen, Scott W., Paradis, Charles, Wu, Liyou, Campbell, James H., Fortney, Julian L., Mehlhorn, Tonia L., Lowe, Kenneth A., Earles, Jennifer E., Phillips, Jana, Techtmann, Steve M., Joyner, Dominique C., Elias, Dwayne A., Bailey, Kathryn L., Hurt, Richard A., Preheim, Sarah P., Sanders, Matthew C., Yang, Joy, Mueller, Marcella A., Brooks, Scott, Watson, David B., Zhang, Ping, He, Zhili, Dubinsky, Eric A., Adams, Paul D., Arkin, Adam P., Fields, Matthew W., Zhou, Jizhong, Alm, Eric J., and Hazen, Terry C. Tue . "Natural bacterial communities serve as quantitative geochemical biosensors". United States. doi:10.1128/mBio.00326-15. https://www.osti.gov/servlets/purl/1215642.
@article{osti_1215642,
title = {Natural bacterial communities serve as quantitative geochemical biosensors},
author = {Smith, Mark B. and Rocha, Andrea M. and Smillie, Chris S. and Olesen, Scott W. and Paradis, Charles and Wu, Liyou and Campbell, James H. and Fortney, Julian L. and Mehlhorn, Tonia L. and Lowe, Kenneth A. and Earles, Jennifer E. and Phillips, Jana and Techtmann, Steve M. and Joyner, Dominique C. and Elias, Dwayne A. and Bailey, Kathryn L. and Hurt, Richard A. and Preheim, Sarah P. and Sanders, Matthew C. and Yang, Joy and Mueller, Marcella A. and Brooks, Scott and Watson, David B. and Zhang, Ping and He, Zhili and Dubinsky, Eric A. and Adams, Paul D. and Arkin, Adam P. and Fields, Matthew W. and Zhou, Jizhong and Alm, Eric J. and Hazen, Terry C.},
abstractNote = {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. 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.},
doi = {10.1128/mBio.00326-15},
journal = {mBio (Online)},
number = 3,
volume = 6,
place = {United States},
year = {Tue May 12 00:00:00 EDT 2015},
month = {Tue May 12 00:00:00 EDT 2015}
}

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Cited by: 17works
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  • We report that 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 memorymore » 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.« less
  • Molecular innovations in microbial ecology are allowing scientists to correlate microbial community characteristics to a variety of ecosystem functions. However, to date the majority of soil microbial ecology studies target phylogenetic rRNA markers, while a smaller number target functional markers linked to soil processes. We validated a new primer set targeting citrate synthase (gtlA), a central enzyme in the citric acid cycle linked to aerobic respiration. Primers for a 225 bp fragment suitable for qPCR were tested for specificity and assay performance verified on multiple soils. Clone libraries of the PCR-amplified gtlA gene exhibited high diversity and recovered most majormore » groups identified in a previous 16S rRNA gene study. Comparisons among bacterial communities based on gtlA sequencing using UniFrac revealed differences among the experimental soils studied. Conditions for gtlA qPCR were optimized and calibration curves were highly linear (R2 > 0.99) over six orders of magnitude (4.56 10^5 to 4.56 10^11 copies), with high amplification efficiencies (>1.7). We examined the performance of the gtlA qPCR across a variety of soils and ecosystems, spanning forests, old fields and agricultural areas. We were able to amplify gtlA genes in all tested soils, and detected differences in gtlA abundance within and among environments. These results indicate that a fully developed gtlA-targeted qPCR approach may have potential to link microbial community characteristics with changes in soil respiration.« less
  • Springtime ozone depletion and the resultant increase in ultraviolet-B (UV-B) radiation [280-320 nanometers (nm)] have deleterious effects on primary productivity. To assess damage to cellular components other than the photosynthetic apparatus, we isolated total community DNA from samples in the field before, during, and after the 1993 springtime depletion in stratospheric ozone. The effort was motivated by the concern that the ozone-dependent increases in UV-B radiation may increase DNA damage within primary producers. This increase in damage could result in changes of species composition as well as hereditary changes within species that can influence the competitiveness of these organisms inmore » their natural community. Previous studies have focused on DNA damage in isolated cultures of antarctic phytoplankton that were irradiated with UV-B under lab conditions. These studies clearly indicate variable species sensitivities to the increase in UV-B flux. These studies, however, did not resolve the question of whether such damage occurred in field samples collected from actively mixing, polyphyletic phytoplankton communities. Potential species composition changes and the resultant changes in the trophic dynamics cannot be interpreted in terms of DNA damage unless this damage can be documented in samples isolated under these dynamic natural conditions. 7 refs., 2 figs.« less
  • Most marine bacteria produce exopolysaccharides (EPS), and bacterial EPS represent an important source of dissolved organic carbon in marine ecosystems. It was proposed that bacterial EPS rich in uronic acid is resistant to mineralization by microbes and thus has a long residence time in global oceans. To confirm this hypothesis, bacterial EPS rich in galacturonic acid was isolated from Alteromonas sp. JL2810. The EPS was used to amend natural seawater to investigate the bioavailability of this EPS by native populations, in the presence and absence of ammonium and phosphate amendment. The data indicated that the bacterial EPS could not bemore » completely consumed during the cultivation period and that the bioavailability of EPS was not only determined by its intrinsic properties, but was also determined by other factors such as the availability of inorganic nutrients. During the experiment, the humic-like component of fluorescent dissolved organic matter (FDOM) was freshly produced. Bacterial community structure analysis indicated that the class Flavobacteria of the phylum Bacteroidetes was the major contributor for the utilization of EPS. This report is the first to indicate that Flavobacteria are a major contributor to bacterial EPS degradation. Finally, the fraction of EPS that could not be completely utilized and the FDOM (e.g., humic acid-like substances) produced de novo may be refractory and may contribute to the carbon storage in the oceans.« less
  • Nitrogen (N) deposition affects myriad aspects of terrestrial ecosystem structure and function, and microbial communities may be particularly sensitive to anthropogenic N inputs. However, our understanding of N deposition effects on microbial communities is far from complete, especially for drylands where data are comparatively rare. To address the need for an improved understanding of dryland biological responses to N deposition, we conducted a two-year fertilization experiment in a semiarid grassland on the Colorado Plateau in the southwestern United States. We evaluated effects of varied levels of N inputs on archaeal, bacterial, fungal and chlorophyte community composition within three microhabitats: biologicalmore » soil crusts (biocrusts), soil below biocrusts, and the plant rhizosphere. Surprisingly, N addition did not affect the community composition or diversity of any of these microbial groups; however, microbial community composition varied significantly among sampling microhabitats. Further, while plant richness, diversity, and cover showed no response to N addition, there were strong linkages between plant properties and microbial community structure. Overall, these findings highlight the potential for some dryland communities to have limited biotic ability to retain augmented N inputs, possibly leading to large N losses to the atmosphere and to aquatic systems.« less