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...

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Autores principales:	Ankita Kothari, Yu-Wei Wu, John-Marc Chandonia, Marimikel Charrier, Lara Rajeev, Andrea M. Rocha, Dominique C. Joyner, Terry C. Hazen, Steven W. Singer, Aindrila Mukhopadhyay
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	antibiotic resistance mer mercury resistance metal resistance native plasmids plasmidome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/485f429716ae4f7e8f9cf5acde61517c
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spelling	oai:doaj.org-article:485f429716ae4f7e8f9cf5acde61517c2021-11-15T15:55:14ZLarge Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes10.1128/mBio.02899-182150-7511https://doaj.org/article/485f429716ae4f7e8f9cf5acde61517c2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02899-18https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Plasmidomes have been typically studied in environments abundant in bacteria, and this is the first study to explore plasmids from an environment characterized by low cell density. We specifically target groundwater, a significant source of water for human/agriculture use. We used samples from a well-studied site and identified hundreds of circular plasmids, including one of the largest sizes reported in plasmidome studies. The striking similarity of the plasmid-borne ORFs in terms of taxonomical and functional classifications across several samples suggests a conserved plasmid pool, in contrast to the observed variability in the 16S rRNA-based microbiome distribution. Additionally, the stress response to environmental factors has stronger conservation via plasmid-borne genes as marked by abundance of metal resistance genes. Last, identification of novel and diverse plasmids enriches the existing plasmid database(s) and serves as a paradigm to increase the repertoire of biological parts that are available for modifying novel environmental strains.Ankita KothariYu-Wei WuJohn-Marc ChandoniaMarimikel CharrierLara RajeevAndrea M. RochaDominique C. JoynerTerry C. HazenSteven W. SingerAindrila MukhopadhyayAmerican Society for Microbiologyarticleantibiotic resistancemermercury resistancemetal resistancenative plasmidsplasmidomeMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	antibiotic resistance mer mercury resistance metal resistance native plasmids plasmidome Microbiology QR1-502
spellingShingle	antibiotic resistance mer mercury resistance metal resistance native plasmids plasmidome Microbiology QR1-502 Ankita Kothari Yu-Wei Wu John-Marc Chandonia Marimikel Charrier Lara Rajeev Andrea M. Rocha Dominique C. Joyner Terry C. Hazen Steven W. Singer Aindrila Mukhopadhyay Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
description	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 role of the plasmidome in maintaining the latent capacity of a microbiome, enabling rapid adaptation to environmental stresses. IMPORTANCE Plasmidomes have been typically studied in environments abundant in bacteria, and this is the first study to explore plasmids from an environment characterized by low cell density. We specifically target groundwater, a significant source of water for human/agriculture use. We used samples from a well-studied site and identified hundreds of circular plasmids, including one of the largest sizes reported in plasmidome studies. The striking similarity of the plasmid-borne ORFs in terms of taxonomical and functional classifications across several samples suggests a conserved plasmid pool, in contrast to the observed variability in the 16S rRNA-based microbiome distribution. Additionally, the stress response to environmental factors has stronger conservation via plasmid-borne genes as marked by abundance of metal resistance genes. Last, identification of novel and diverse plasmids enriches the existing plasmid database(s) and serves as a paradigm to increase the repertoire of biological parts that are available for modifying novel environmental strains.
format	article
author	Ankita Kothari Yu-Wei Wu John-Marc Chandonia Marimikel Charrier Lara Rajeev Andrea M. Rocha Dominique C. Joyner Terry C. Hazen Steven W. Singer Aindrila Mukhopadhyay
author_facet	Ankita Kothari Yu-Wei Wu John-Marc Chandonia Marimikel Charrier Lara Rajeev Andrea M. Rocha Dominique C. Joyner Terry C. Hazen Steven W. Singer Aindrila Mukhopadhyay
author_sort	Ankita Kothari
title	Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
title_short	Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
title_full	Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
title_fullStr	Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
title_full_unstemmed	Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
title_sort	large circular plasmids from groundwater plasmidomes span multiple incompatibility groups and are enriched in multimetal resistance genes
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/485f429716ae4f7e8f9cf5acde61517c
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Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes

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