Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil
Abstract
Soils are reservoirs of antibiotic resistance genes (ARGs), but environmental dynamics of ARGs are largely unknown. Long-term disturbances offer opportunities to examine microbiome responses at scales relevant for both ecological and evolutionary processes and can be insightful for studying ARGs. We examined ARGs in soils overlying the underground coal seam fire in Centralia, PA, which has been burning since 1962. As the fire progresses, previously hot soils can recover to ambient temperatures, which creates a gradient of fire impact. We examined metagenomes from surface soils along this gradient to examine ARGs using a gene-targeted assembler. We targeted 35 clinically relevant ARGs and two horizontal gene transfer-related genes (intI and repA). We detected 17 ARGs in Centralia: AAC6-Ia, adeB, bla_A, bla_B, bla_C, cmlA, dfra12, intI, sul2, tetA, tetW, tetX, tolC, vanA, vanH, vanX and vanZ. The diversity and abundance of bla_A, bla_B, dfra12 and tolC decreased with soil temperature, and changes in ARGs were largely explained by changes in community structure. We observed sequence-specific biogeography along the temperature gradient and observed compositional shifts in bla_A, dfra12 and intI. These results suggest that increased temperatures can reduce soil ARGs but that this is largely due to a concomitant reduction in community-level diversity.
- Authors:
-
- Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA, Environmental and Integrative Toxicological Sciences Doctoral Program, Michigan State University, East Lansing, MI 48824, USA
- Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA, Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI 48824, USA, Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI 48824, USA
- Publication Date:
- Research Org.:
- USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1457202
- Alternate Identifier(s):
- OSTI ID: 1904110
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- FEMS Microbiology Ecology (Online)
- Additional Journal Information:
- Journal Name: FEMS Microbiology Ecology (Online) Journal Volume: 94 Journal Issue: 3; Journal ID: ISSN 1574-6941
- Publisher:
- Oxford University Press
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; thermophile; gene-targeted assembly; metagenome; rplB; coal fire
Citation Formats
Dunivin, T. K., and Shade, A. Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil. Netherlands: N. p., 2018.
Web. doi:10.1093/femsec/fiy016.
Dunivin, T. K., & Shade, A. Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil. Netherlands. https://doi.org/10.1093/femsec/fiy016
Dunivin, T. K., and Shade, A. Thu .
"Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil". Netherlands. https://doi.org/10.1093/femsec/fiy016.
@article{osti_1457202,
title = {Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil},
author = {Dunivin, T. K. and Shade, A.},
abstractNote = {Soils are reservoirs of antibiotic resistance genes (ARGs), but environmental dynamics of ARGs are largely unknown. Long-term disturbances offer opportunities to examine microbiome responses at scales relevant for both ecological and evolutionary processes and can be insightful for studying ARGs. We examined ARGs in soils overlying the underground coal seam fire in Centralia, PA, which has been burning since 1962. As the fire progresses, previously hot soils can recover to ambient temperatures, which creates a gradient of fire impact. We examined metagenomes from surface soils along this gradient to examine ARGs using a gene-targeted assembler. We targeted 35 clinically relevant ARGs and two horizontal gene transfer-related genes (intI and repA). We detected 17 ARGs in Centralia: AAC6-Ia, adeB, bla_A, bla_B, bla_C, cmlA, dfra12, intI, sul2, tetA, tetW, tetX, tolC, vanA, vanH, vanX and vanZ. The diversity and abundance of bla_A, bla_B, dfra12 and tolC decreased with soil temperature, and changes in ARGs were largely explained by changes in community structure. We observed sequence-specific biogeography along the temperature gradient and observed compositional shifts in bla_A, dfra12 and intI. These results suggest that increased temperatures can reduce soil ARGs but that this is largely due to a concomitant reduction in community-level diversity.},
doi = {10.1093/femsec/fiy016},
journal = {FEMS Microbiology Ecology (Online)},
number = 3,
volume = 94,
place = {Netherlands},
year = {Thu Feb 01 00:00:00 EST 2018},
month = {Thu Feb 01 00:00:00 EST 2018}
}
https://doi.org/10.1093/femsec/fiy016
Web of Science
Works referenced in this record:
Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets
journal, October 2013
- Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
- Bioinformatics, Vol. 30, Issue 5
Call of the wild: antibiotic resistance genes in natural environments
journal, March 2010
- Allen, Heather K.; Donato, Justin; Wang, Helena Huimi
- Nature Reviews Microbiology, Vol. 8, Issue 4
Antibiotic resistance genes in manure-amended soil and vegetables at harvest
journal, December 2015
- Wang, Feng-Hua; Qiao, Min; Chen, Zheng
- Journal of Hazardous Materials, Vol. 299
Novel Florfenicol and Chloramphenicol Resistance Gene Discovered in Alaskan Soil by Using Functional Metagenomics
journal, June 2010
- Lang, K. S.; Anderson, J. M.; Schwarz, S.
- Applied and Environmental Microbiology, Vol. 76, Issue 15
Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection
journal, December 2016
- Li, Li-Guan; Xia, Yu; Zhang, Tong
- The ISME Journal, Vol. 11, Issue 3
Diversity of gene cassettes and the abundance of the class 1 integron-integrase gene in sediment polluted by metals
journal, March 2016
- Oliveira-Pinto, Clarisse; Costa, Patrícia S.; Reis, Mariana P.
- Extremophiles, Vol. 20, Issue 3
Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012
- Shade, Ashley; Peter, Hannes; Allison, Steven D.
- Frontiers in Microbiology, Vol. 3
Metagenomic profiling of historic Colorado Front Range flood impact on distribution of riverine antibiotic resistance genes
journal, December 2016
- Garner, Emily; Wallace, Joshua S.; Argoty, Gustavo Arango
- Scientific Reports, Vol. 6, Issue 1
FunGene: the functional gene pipeline and repository
journal, January 2013
- Fish, Jordan A.; Chai, Benli; Wang, Qiong
- Frontiers in Microbiology, Vol. 4
Xander: employing a novel method for efficient gene-targeted metagenomic assembly
journal, August 2015
- Wang, Qiong; Fish, Jordan A.; Gilman, Mariah
- Microbiome, Vol. 3, Issue 1
Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential
journal, November 2015
- Pal, Chandan; Bengtsson-Palme, Johan; Kristiansson, Erik
- BMC Genomics, Vol. 16, Issue 1
Changes of resistome, mobilome and potential hosts of antibiotic resistance genes during the transformation of anaerobic digestion from mesophilic to thermophilic
journal, July 2016
- Tian, Zhe; Zhang, Yu; Yu, Bo
- Water Research, Vol. 98
Community Genomic and Proteomic Analyses of Chemoautotrophic Iron-Oxidizing "Leptospirillum rubarum" (Group II) and "Leptospirillum ferrodiazotrophum" (Group III) Bacteria in Acid Mine Drainage Biofilms
journal, May 2009
- Goltsman, D. S. A.; Denef, V. J.; Singer, S. W.
- Applied and Environmental Microbiology, Vol. 75, Issue 13
The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria: The soil resistome
journal, December 2014
- Nesme, Joseph; Simonet, Pascal
- Environmental Microbiology, Vol. 17, Issue 4
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, Issue 1
Effect of Temperature on the Fate of Genes Encoding Tetracycline Resistance and the Integrase of Class 1 Integrons within Anaerobic and Aerobic Digesters Treating Municipal Wastewater Solids
journal, December 2010
- Diehl, David L.; LaPara, Timothy M.
- Environmental Science & Technology, Vol. 44, Issue 23
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Tackling antibiotic resistance: the environmental framework
journal, March 2015
- Berendonk, Thomas U.; Manaia, Célia M.; Merlin, Christophe
- Nature Reviews Microbiology, Vol. 13, Issue 5
Coping with copper: legacy effect of copper on potential activity of soil bacteria following a century of exposure
journal, August 2016
- Nunes, Inês; Jacquiod, Samuel; Brejnrod, Asker
- FEMS Microbiology Ecology, Vol. 92, Issue 11
Mapping the coal fire at Centralia, Pa using thermal infrared imagery
journal, September 2011
- Elick, Jennifer M.
- International Journal of Coal Geology, Vol. 87, Issue 3-4
Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review
journal, March 2013
- Rizzo, L.; Manaia, C.; Merlin, C.
- Science of The Total Environment, Vol. 447
Evolution and ecology of antibiotic resistance genes
journal, June 2007
- Aminov, Rustam I.; Mackie, Roderick I.
- FEMS Microbiology Letters, Vol. 271, Issue 2
Antibiotic resistance genes across a wide variety of metagenomes
journal, January 2016
- Fitzpatrick, David; Walsh, Fiona
- FEMS Microbiology Ecology, Vol. 92, Issue 2
Bacterial phylogeny structures soil resistomes across habitats
journal, May 2014
- Forsberg, Kevin J.; Patel, Sanket; Gibson, Molly K.
- Nature, Vol. 509, Issue 7502
VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R
journal, January 2011
- Chen, Hanbo; Boutros, Paul C.
- BMC Bioinformatics, Vol. 12, Issue 1
Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fire
journal, March 2017
- Lee, Sang-Hoon; Sorensen, Jackson W.; Grady, Keara L.
- The ISME Journal, Vol. 11, Issue 6
Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting
journal, November 2016
- Qian, Xun; Sun, Wei; Gu, Jie
- Bioresource Technology, Vol. 220
Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans
journal, May 2011
- Wannaprasat, Wechsiri; Padungtod, Pawin; Chuanchuen, Rungtip
- International Journal of Antimicrobial Agents, Vol. 37, Issue 5
Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
journal, April 2016
- Johnson, Timothy A.; Stedtfeld, Robert D.; Wang, Qiong
- mBio, Vol. 7, Issue 2
Coal mine fires and human health: What do we know?
journal, December 2015
- Melody, S. M.; Johnston, F. H.
- International Journal of Coal Geology, Vol. 152
Acquired Antibiotic Resistance Genes: An Overview
journal, January 2011
- van Hoek, Angela H. A. M.; Mevius, Dik; Guerra, Beatriz
- Frontiers in Microbiology, Vol. 2
Antibiotic resistance in the wild: an eco-evolutionary perspective
journal, January 2017
- Hiltunen, Teppo; Virta, Marko; Laine, Anna-Liisa
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1712
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Cross-biome metagenomic analyses of soil microbial communities and their functional attributes
journal, December 2012
- Fierer, N.; Leff, J. W.; Adams, B. J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 52