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Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil

BACKGROUND: Cupriavidus strain STM 6070 was isolated from nickel-rich soil collected near Koniambo massif, New Caledonia, using the invasive legume trap host Mimosa pudica. STM 6070 is a heavy metal-tolerant strain that is highly effective at fixing nitrogen with M. pudica. Here we have provided an...

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Autores principales: Klonowska, Agnieszka, Moulin, Lionel, Ardley, Julie Kaye, Braun, Florence, Gollagher, Margaret Mary, Zandberg, Jaco Daniel, Marinova, Dora Vasileva, Huntemann, Marcel, Reddy, T. B. K., Varghese, Neha Jacob, Woyke, Tanja, Ivanova, Natalia, Seshadri, Rekha, Kyrpides, Nikos, Reeve, Wayne Gerald
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7060636/
https://www.ncbi.nlm.nih.gov/pubmed/32143559
http://dx.doi.org/10.1186/s12864-020-6623-z
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author Klonowska, Agnieszka
Moulin, Lionel
Ardley, Julie Kaye
Braun, Florence
Gollagher, Margaret Mary
Zandberg, Jaco Daniel
Marinova, Dora Vasileva
Huntemann, Marcel
Reddy, T. B. K.
Varghese, Neha Jacob
Woyke, Tanja
Ivanova, Natalia
Seshadri, Rekha
Kyrpides, Nikos
Reeve, Wayne Gerald
author_facet Klonowska, Agnieszka
Moulin, Lionel
Ardley, Julie Kaye
Braun, Florence
Gollagher, Margaret Mary
Zandberg, Jaco Daniel
Marinova, Dora Vasileva
Huntemann, Marcel
Reddy, T. B. K.
Varghese, Neha Jacob
Woyke, Tanja
Ivanova, Natalia
Seshadri, Rekha
Kyrpides, Nikos
Reeve, Wayne Gerald
author_sort Klonowska, Agnieszka
collection PubMed
description BACKGROUND: Cupriavidus strain STM 6070 was isolated from nickel-rich soil collected near Koniambo massif, New Caledonia, using the invasive legume trap host Mimosa pudica. STM 6070 is a heavy metal-tolerant strain that is highly effective at fixing nitrogen with M. pudica. Here we have provided an updated taxonomy for STM 6070 and described salient features of the annotated genome, focusing on heavy metal resistance (HMR) loci and heavy metal efflux (HME) systems. RESULTS: The 6,771,773 bp high-quality-draft genome consists of 107 scaffolds containing 6118 protein-coding genes. ANI values show that STM 6070 is a new species of Cupriavidus. The STM 6070 symbiotic region was syntenic with that of the M. pudica-nodulating Cupriavidus taiwanensis LMG 19424(T). In contrast to the nickel and zinc sensitivity of C. taiwanensis strains, STM 6070 grew at high Ni(2+) and Zn(2+) concentrations. The STM 6070 genome contains 55 genes, located in 12 clusters, that encode HMR structural proteins belonging to the RND, MFS, CHR, ARC3, CDF and P-ATPase protein superfamilies. These HMR molecular determinants are putatively involved in arsenic (ars), chromium (chr), cobalt-zinc-cadmium (czc), copper (cop, cup), nickel (nie and nre), and silver and/or copper (sil) resistance. Seven of these HMR clusters were common to symbiotic and non-symbiotic Cupriavidus species, while four clusters were specific to STM 6070, with three of these being associated with insertion sequences. Within the specific STM 6070 HMR clusters, three novel HME-RND systems (nieIC cep nieBA, czcC2B2A2, and hmxB zneAC zneR hmxS) were identified, which constitute new candidate genes for nickel and zinc resistance. CONCLUSIONS: STM 6070 belongs to a new Cupriavidus species, for which we have proposed the name Cupriavidus neocaledonicus sp. nov.. STM6070 harbours a pSym with a high degree of gene conservation to the pSyms of M. pudica-nodulating C. taiwanensis strains, probably as a result of recent horizontal transfer. The presence of specific HMR clusters, associated with transposase genes, suggests that the selection pressure of the New Caledonian ultramafic soils has driven the specific adaptation of STM 6070 to heavy-metal-rich soils via horizontal gene transfer.
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spelling pubmed-70606362020-03-12 Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil Klonowska, Agnieszka Moulin, Lionel Ardley, Julie Kaye Braun, Florence Gollagher, Margaret Mary Zandberg, Jaco Daniel Marinova, Dora Vasileva Huntemann, Marcel Reddy, T. B. K. Varghese, Neha Jacob Woyke, Tanja Ivanova, Natalia Seshadri, Rekha Kyrpides, Nikos Reeve, Wayne Gerald BMC Genomics Research Article BACKGROUND: Cupriavidus strain STM 6070 was isolated from nickel-rich soil collected near Koniambo massif, New Caledonia, using the invasive legume trap host Mimosa pudica. STM 6070 is a heavy metal-tolerant strain that is highly effective at fixing nitrogen with M. pudica. Here we have provided an updated taxonomy for STM 6070 and described salient features of the annotated genome, focusing on heavy metal resistance (HMR) loci and heavy metal efflux (HME) systems. RESULTS: The 6,771,773 bp high-quality-draft genome consists of 107 scaffolds containing 6118 protein-coding genes. ANI values show that STM 6070 is a new species of Cupriavidus. The STM 6070 symbiotic region was syntenic with that of the M. pudica-nodulating Cupriavidus taiwanensis LMG 19424(T). In contrast to the nickel and zinc sensitivity of C. taiwanensis strains, STM 6070 grew at high Ni(2+) and Zn(2+) concentrations. The STM 6070 genome contains 55 genes, located in 12 clusters, that encode HMR structural proteins belonging to the RND, MFS, CHR, ARC3, CDF and P-ATPase protein superfamilies. These HMR molecular determinants are putatively involved in arsenic (ars), chromium (chr), cobalt-zinc-cadmium (czc), copper (cop, cup), nickel (nie and nre), and silver and/or copper (sil) resistance. Seven of these HMR clusters were common to symbiotic and non-symbiotic Cupriavidus species, while four clusters were specific to STM 6070, with three of these being associated with insertion sequences. Within the specific STM 6070 HMR clusters, three novel HME-RND systems (nieIC cep nieBA, czcC2B2A2, and hmxB zneAC zneR hmxS) were identified, which constitute new candidate genes for nickel and zinc resistance. CONCLUSIONS: STM 6070 belongs to a new Cupriavidus species, for which we have proposed the name Cupriavidus neocaledonicus sp. nov.. STM6070 harbours a pSym with a high degree of gene conservation to the pSyms of M. pudica-nodulating C. taiwanensis strains, probably as a result of recent horizontal transfer. The presence of specific HMR clusters, associated with transposase genes, suggests that the selection pressure of the New Caledonian ultramafic soils has driven the specific adaptation of STM 6070 to heavy-metal-rich soils via horizontal gene transfer. BioMed Central 2020-03-06 /pmc/articles/PMC7060636/ /pubmed/32143559 http://dx.doi.org/10.1186/s12864-020-6623-z Text en © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Klonowska, Agnieszka
Moulin, Lionel
Ardley, Julie Kaye
Braun, Florence
Gollagher, Margaret Mary
Zandberg, Jaco Daniel
Marinova, Dora Vasileva
Huntemann, Marcel
Reddy, T. B. K.
Varghese, Neha Jacob
Woyke, Tanja
Ivanova, Natalia
Seshadri, Rekha
Kyrpides, Nikos
Reeve, Wayne Gerald
Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title_full Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title_fullStr Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title_full_unstemmed Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title_short Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
title_sort novel heavy metal resistance gene clusters are present in the genome of cupriavidus neocaledonicus stm 6070, a new species of mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7060636/
https://www.ncbi.nlm.nih.gov/pubmed/32143559
http://dx.doi.org/10.1186/s12864-020-6623-z
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