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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

Abstract

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 19424T. In contrast to the nickel and zinc sensitivity of C. taiwanensis strains, STM 6070 grew at high Ni2+ and Zn2+ 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-symbioticmore » 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.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); French National Agency of Research; Curtin Univ. Sustainability Policy Inst.; Murdoch Univ.
OSTI Identifier:
1618578
Alternate Identifier(s):
OSTI ID: 1615317
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Name: BMC Genomics Journal Volume: 21 Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Rhizobia; Cupriavidus; Nickel tolerance; HGT; Mimosa; Rhizobial biogeography; Heavy metal resistance; Heavy metal efflux

Citation Formats

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, and 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. United Kingdom: N. p., 2020. Web. doi:10.1186/s12864-020-6623-z.
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. United Kingdom. doi:https://doi.org/10.1186/s12864-020-6623-z
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, and Reeve, Wayne Gerald. Fri . "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". United Kingdom. doi:https://doi.org/10.1186/s12864-020-6623-z.
@article{osti_1618578,
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},
author = {Klonowska, Agnieszka and Moulin, Lionel and Ardley, Julie Kaye and Braun, Florence and Gollagher, Margaret Mary and Zandberg, Jaco Daniel and Marinova, Dora Vasileva and Huntemann, Marcel and Reddy, T. B. K. and Varghese, Neha Jacob and Woyke, Tanja and Ivanova, Natalia and Seshadri, Rekha and Kyrpides, Nikos and Reeve, Wayne Gerald},
abstractNote = {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 19424T. In contrast to the nickel and zinc sensitivity of C. taiwanensis strains, STM 6070 grew at high Ni2+ and Zn2+ 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.},
doi = {10.1186/s12864-020-6623-z},
journal = {BMC Genomics},
number = 1,
volume = 21,
place = {United Kingdom},
year = {2020},
month = {3}
}

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DOI: https://doi.org/10.1186/s12864-020-6623-z

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