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Title: Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes

Abstract

Naturally occurring plasmids constitute a major category of mobile genetic elements responsible for harboring and transferring genes important in survival and fitness. A targeted evaluation of plasmidomes can reveal unique adaptations required by microbial communities. We developed a model system to optimize plasmid DNA isolation procedures targeted to groundwater samples which are typically characterized by low cell density (and likely variations in the plasmid size and copy numbers). The optimized method resulted in successful identification of several hundred circular plasmids, including some large plasmids (11 plasmids more than 50 kb in size, with the largest being 1.7 Mb in size). Several interesting observations were made from the analysis of plasmid DNA isolated in this study. The plasmid pool (plasmidome) was more conserved than the corresponding microbiome distribution (16S rRNA based). The circular plasmids were diverse as represented by the presence of seven plasmid incompatibility groups. The genes carried on these groundwater plasmids were highly enriched in metal resistance. Results from this study confirmed that traits such as metal, antibiotic, and phage resistance along with toxin-antitoxin systems are encoded on abundant circular plasmids, all of which could confer novel and advantageous traits to their hosts. This study confirms the ecological rolemore » of the plasmidome in maintaining the latent capacity of a microbiome, enabling rapid adaptation to environmental stresses.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [1]; ORCiD logo [1];  [1];  [3];  [4]; ORCiD logo [5];  [1]; ORCiD logo [1]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Taipei Medical University (Taiwan)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1496501
Alternate Identifier(s):
OSTI ID: 1528692; OSTI ID: 1545317
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kothari, Ankita, Wu, Yu-Wei, Chandonia, John-Marc, Charrier, Marimikel, Rajeev, Lara, Rocha, Andrea M., Joyner, Dominique C., Hazen, Terry C., Singer, Steven W., and Mukhopadhyay, Aindrila. Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes. United States: N. p., 2019. Web. doi:10.1128/mBio.02899-18.
Kothari, Ankita, Wu, Yu-Wei, Chandonia, John-Marc, Charrier, Marimikel, Rajeev, Lara, Rocha, Andrea M., Joyner, Dominique C., Hazen, Terry C., Singer, Steven W., & Mukhopadhyay, Aindrila. Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes. United States. doi:10.1128/mBio.02899-18.
Kothari, Ankita, Wu, Yu-Wei, Chandonia, John-Marc, Charrier, Marimikel, Rajeev, Lara, Rocha, Andrea M., Joyner, Dominique C., Hazen, Terry C., Singer, Steven W., and Mukhopadhyay, Aindrila. Tue . "Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes". United States. doi:10.1128/mBio.02899-18.
@article{osti_1496501,
title = {Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes},
author = {Kothari, Ankita and Wu, Yu-Wei and Chandonia, John-Marc and Charrier, Marimikel and Rajeev, Lara and Rocha, Andrea M. and Joyner, Dominique C. and Hazen, Terry C. and Singer, Steven W. and Mukhopadhyay, Aindrila},
abstractNote = {Naturally occurring plasmids constitute a major category of mobile genetic elements responsible for harboring and transferring genes important in survival and fitness. A targeted evaluation of plasmidomes can reveal unique adaptations required by microbial communities. We developed a model system to optimize plasmid DNA isolation procedures targeted to groundwater samples which are typically characterized by low cell density (and likely variations in the plasmid size and copy numbers). The optimized method resulted in successful identification of several hundred circular plasmids, including some large plasmids (11 plasmids more than 50 kb in size, with the largest being 1.7 Mb in size). Several interesting observations were made from the analysis of plasmid DNA isolated in this study. The plasmid pool (plasmidome) was more conserved than the corresponding microbiome distribution (16S rRNA based). The circular plasmids were diverse as represented by the presence of seven plasmid incompatibility groups. The genes carried on these groundwater plasmids were highly enriched in metal resistance. Results from this study confirmed that traits such as metal, antibiotic, and phage resistance along with toxin-antitoxin systems are encoded on abundant circular plasmids, all of which could confer novel and advantageous traits to their hosts. This study confirms the ecological role of the plasmidome in maintaining the latent capacity of a microbiome, enabling rapid adaptation to environmental stresses.},
doi = {10.1128/mBio.02899-18},
journal = {mBio (Online)},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1128/mBio.02899-18

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Works referenced in this record:

Search and clustering orders of magnitude faster than BLAST
journal, August 2010