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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. 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. 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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s12864-020-6623-z

Figures / Tables:

Table 1 Table 1 : Genome Statistics for Cupriavidus strain STM 6070

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Works referenced in this record:

FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress
journal, November 2004


Putative cobalt- and nickel-binding proteins and motifs in Streptococcus pneumoniae
journal, January 2013

  • Sun, Xuesong; Yu, Guangchuang; Xu, Qian
  • Metallomics, Vol. 5, Issue 7
  • DOI: 10.1039/c3mt00126a

Burkholderia species are ancient symbionts of legumes
journal, January 2010


Molecular Analysis of the Copper-Transporting Efflux System CusCFBA of Escherichia coli
journal, July 2003


A Gene Cluster Involved in Metal Homeostasis in the Cyanobacterium Synechocystis sp. Strain PCC 6803
journal, March 2000


Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems
journal, June 2010

  • De Angelis, F.; Lee, J. K.; O'Connell, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
  • DOI: 10.1073/pnas.1003908107

Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient
journal, September 2001

  • Chen, W. M.; Laevens, S.; Lee, T. M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 51, Issue 5
  • DOI: 10.1099/00207713-51-5-1729

New Betaproteobacterial Rhizobium Strains Able To Efficiently Nodulate Parapiptadenia rigida (Benth.) Brenan
journal, January 2012

  • Taulé, Cecilia; Zabaleta, María; Mareque, Cintia
  • Applied and Environmental Microbiology, Vol. 78, Issue 6
  • DOI: 10.1128/AEM.06215-11

The evolutionary history of Mimosa (Leguminosae): Toward a phylogeny of the sensitive plants
journal, July 2011

  • Simon, Marcelo F.; Grether, Rosaura; de Queiroz, Luciano P.
  • American Journal of Botany, Vol. 98, Issue 7
  • DOI: 10.3732/ajb.1000520

ArsR arsenic-resistance regulatory protein from Cupriavidus metallidurans CH34
journal, February 2009

  • Zhang, Yian-Biao; Monchy, Sébastien; Greenberg, Bill
  • Antonie van Leeuwenhoek, Vol. 96, Issue 2
  • DOI: 10.1007/s10482-009-9313-z

An invasive Mimosa in India does not adopt the symbionts of its native relatives
journal, May 2013

  • Gehlot, Hukam Singh; Tak, Nisha; Kaushik, Muskan
  • Annals of Botany, Vol. 112, Issue 1
  • DOI: 10.1093/aob/mct112

MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data
journal, November 2012

  • Vallenet, David; Belda, Eugeni; Calteau, Alexandra
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1194

A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803
journal, January 2002


High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010

  • Gnerre, S.; MacCallum, I.; Przybylski, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
  • DOI: 10.1073/pnas.1017351108

Solexa Ltd
journal, June 2004


Ralstonia metallidurans , a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes
journal, June 2003


Escherichia coli mechanisms of copper homeostasis in a changing environment
journal, June 2003


TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels
journal, January 2007

  • Ren, Q.; Chen, K.; Paulsen, I. T.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl925

New genes involved in chromate resistance inRalstonia metallidurans strain CH34
journal, January 2002

  • Juhnke, Susanne; Peitzsch, Nicola; Hübener, Nicole
  • Archives of Microbiology, Vol. 179, Issue 1
  • DOI: 10.1007/s00203-002-0492-5

Novel Bacterial P-Type ATPases with Histidine-Rich Heavy-Metal-Associated Sequences
journal, December 1994

  • Trenor, C.; Lin, W.; Andrews, N. C.
  • Biochemical and Biophysical Research Communications, Vol. 205, Issue 3
  • DOI: 10.1006/bbrc.1994.2856

tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997


Genome sequence of the plant pathogen Ralstonia solanacearum
journal, January 2002

  • Salanoubat, M.; Genin, S.; Artiguenave, F.
  • Nature, Vol. 415, Issue 6871
  • DOI: 10.1038/415497a

Genome Analysis of Minibacterium massiliensis Highlights the Convergent Evolution of Water-Living Bacteria
journal, August 2007


The Genomic Standards Consortium
journal, June 2011


Legume-Nodulating Betaproteobacteria: Diversity, Host Range, and Future Prospects
journal, November 2011

  • Gyaneshwar, Prasad; Hirsch, Ann M.; Moulin, Lionel
  • Molecular Plant-Microbe Interactions, Vol. 24, Issue 11
  • DOI: 10.1094/MPMI-06-11-0172

Genome archeology leading to the characterization and classification of transport proteins
journal, October 1999


Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans Are Specialized in the Maximal Viable Response to Heavy Metals
journal, August 2007

  • Monchy, S.; Benotmane, M. A.; Janssen, P.
  • Journal of Bacteriology, Vol. 189, Issue 20
  • DOI: 10.1128/JB.00375-07

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Formation and Utilization of Poly-β-Hydroxybutyric Acid by Knallgas Bacteria (Hydrogenomonas)
journal, July 1961

  • Schlegel, H. G.; Gottschalk, G.; Von Bartha, R.
  • Nature, Vol. 191, Issue 4787
  • DOI: 10.1038/191463a0

New mobile genetic elements in Cupriavidus metallidurans CH34, their possible roles and occurrence in other bacteria
journal, April 2009


Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China
journal, February 2012


IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

Kinase Activity of ArcB from Escherichia coli Is Subject to Regulation by Both Ubiquinone and Demethylmenaquinone
journal, October 2013


Novel Cupriavidus Strains Isolated from Root Nodules of Native Uruguayan Mimosa Species
journal, March 2016

  • Platero, Raúl; James, Euan K.; Rios, Cecilia
  • Applied and Environmental Microbiology, Vol. 82, Issue 11
  • DOI: 10.1128/AEM.04142-15

Ubiquinone and Menaquinone Electron Carriers Represent the Yin and Yang in the Redox Regulation of the ArcB Sensor Kinase
journal, May 2013

  • Alvarez, A. F.; Rodriguez, C.; Georgellis, D.
  • Journal of Bacteriology, Vol. 195, Issue 13
  • DOI: 10.1128/JB.00406-13

Copper resistance in Pseudomonas syringae mediated by periplasmic and outer membrane proteins.
journal, October 1991

  • Cha, J. S.; Cooksey, D. A.
  • Proceedings of the National Academy of Sciences, Vol. 88, Issue 20
  • DOI: 10.1073/pnas.88.20.8915

Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34
journal, June 2006

  • Monchy, Sébastien; Benotmane, Mohammed A.; Wattiez, Ruddy
  • Microbiology, Vol. 152, Issue 6
  • DOI: 10.1099/mic.0.28593-0

The impact of insertion sequences on bacterial genome plasticity and adaptability
journal, April 2017


High-quality permanent draft genome sequence of the Mimosa asperata - nodulating Cupriavidus sp. strain AMP6
journal, October 2015

  • De Meyer, Sofie E.; Parker, Matthew; Van Berkum, Peter
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/s40793-015-0074-1

Complete Genome Sequence of the Type Strain Cupriavidus necator N-1
journal, July 2011

  • Poehlein, A.; Kusian, B.; Friedrich, B.
  • Journal of Bacteriology, Vol. 193, Issue 18
  • DOI: 10.1128/JB.05660-11

Burkholderia Species Are the Most Common and Preferred Nodulating Symbionts of the Piptadenia Group (Tribe Mimoseae)
journal, May 2013


How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model
journal, August 2007

  • Jones, Kathryn M.; Kobayashi, Hajime; Davies, Bryan W.
  • Nature Reviews Microbiology, Vol. 5, Issue 8
  • DOI: 10.1038/nrmicro1705

Phylogenetic analysis of the chromate ion transporter (CHR) superfamily: Chromate ion transporter (CHR) phylogeny
journal, November 2007


progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010


The Chromosomally Encoded Cation Diffusion Facilitator Proteins DmeF and FieF from Wautersia metallidurans CH34 Are Transporters of Broad Metal Specificity
journal, December 2004


Nodulation of legumes by members of the β-subclass of Proteobacteria
journal, June 2001

  • Moulin, Lionel; Munive, Antonio; Dreyfus, Bernard
  • Nature, Vol. 411, Issue 6840
  • DOI: 10.1038/35082070

Burkholderia spp. are the most competitive symbionts of Mimosa , particularly under N-limited conditions
journal, April 2009


High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes
journal, January 2009

  • Henne, Kristene L.; Nakatsu, Cindy H.; Thompson, Dorothea K.
  • BMC Microbiology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2180-9-199

A single sym plasmid type predominates across diverse chromosomal lineages of Cupriavidus nodule symbionts
journal, September 2015


The Transporter Classification Database (TCDB): recent advances
journal, November 2015

  • Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1103

Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals.
journal, January 1985


SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid
journal, April 2010

  • Harrison, Peter W.; Lower, Ryan P. J.; Kim, Nayoung K. D.
  • Trends in Microbiology, Vol. 18, Issue 4
  • DOI: 10.1016/j.tim.2009.12.010

Phylogeny based on 16S rDNA and nifH sequences of Ralstonia taiwanensis strains isolated from nitrogen-fixing nodules of Mimosa pudica , in India
journal, May 2004

  • Verma, Subhash Chandra; Chowdhury, Soumitra Paul; Tripathi, Anil Kumar
  • Canadian Journal of Microbiology, Vol. 50, Issue 5
  • DOI: 10.1139/w04-020

Energetics and Topology of CzcA, a Cation/Proton Antiporter of the Resistance-Nodulation-Cell Division Protein Family
journal, September 1999

  • Goldberg, Martina; Pribyl, Thomas; Juhnke, Susanne
  • Journal of Biological Chemistry, Vol. 274, Issue 37
  • DOI: 10.1074/jbc.274.37.26065

Taxonomy of the genus Cupriavidus: a tale of lost and found
journal, November 2004

  • Vandamme, P.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 6
  • DOI: 10.1099/ijs.0.63247-0

Cupriavidus alkaliphilus sp. nov., a new species associated with agricultural plants that grow in alkaline soils
journal, July 2012

  • Estrada-de los Santos, Paulina; Martínez-Aguilar, Lourdes; López-Lara, Isabel M.
  • Systematic and Applied Microbiology, Vol. 35, Issue 5
  • DOI: 10.1016/j.syapm.2012.05.005

Confidence Limits on Phylogenies: an Approach Using the Bootstrap
journal, July 1985


beta-Rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan
journal, December 2005


Monophyly of nodA and nifH Genes across Texan and Costa Rican Populations of Cupriavidus Nodule Symbionts
journal, May 2007

  • Andam, C. P.; Mondo, S. J.; Parker, M. A.
  • Applied and Environmental Microbiology, Vol. 73, Issue 14
  • DOI: 10.1128/AEM.00160-07

Zinc-Induced Transposition of Insertion Sequence Elements Contributes to Increased Adaptability of Cupriavidus metallidurans
journal, March 2016


Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies
journal, September 2010


A Genomic Encyclopedia of the Root Nodule Bacteria: assessing genetic diversity through a systematic biogeographic survey
journal, February 2015

  • Reeve, Wayne; Ardley, Julie; Tian, Rui
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/1944-3277-10-14

The minimum information about a genome sequence (MIGS) specification
journal, May 2008

  • Field, Dawn; Garrity, George; Gray, Tanya
  • Nature Biotechnology, Vol. 26, Issue 5
  • DOI: 10.1038/nbt1360

Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus.
journal, April 1990


Genome sequence of the  -rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia
journal, July 2008


Efflux-mediated heavy metal resistance in prokaryotes
journal, June 2003


Phylogenetic relationships and diversity of β-rhizobia associated with Mimosa species grown in Sishuangbanna, China
journal, February 2011

  • Liu, Xiao Yun; Wu, Wei; Wang, En Tao
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 61, Issue 2
  • DOI: 10.1099/ijs.0.020560-0

Selective Metal Binding to a Membrane-embedded Aspartate in the Escherichia coli Metal Transporter YiiP (FieF)
journal, July 2005


Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. Nodule Bacteria on two Mimosa spp. in Costa Rica
journal, February 2006


Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network
journal, June 2011


Structures of intermediate transport states of ZneA, a Zn(II)/proton antiporter
journal, October 2013

  • Pak, J. E.; Ekende, E. N.; Kifle, E. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 46
  • DOI: 10.1073/pnas.1318705110

Genome sequence of the bioplastic-producing “Knallgas” bacterium Ralstonia eutropha H16
journal, September 2006

  • Pohlmann, Anne; Fricke, Wolfgang Florian; Reinecke, Frank
  • Nature Biotechnology, Vol. 24, Issue 10
  • DOI: 10.1038/nbt1244

Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils
journal, May 2012


TCDB: the Transporter Classification Database for membrane transport protein analyses and information
journal, January 2006


Cupriavidus pinatubonensis sp. nov. and Cupriavidus laharis sp. nov., novel hydrogen-oxidizing, facultatively chemolithotrophic bacteria isolated from volcanic mudflow deposits from Mt. Pinatubo in the Philippines
journal, May 2006

  • Sato, Yoshinori; Nishihara, Hirofumi; Yoshida, Masao
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 56, Issue 5
  • DOI: 10.1099/ijs.0.63922-0

Metal biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica
journal, March 2008


Discovery of Novel Plant Interaction Determinants from the Genomes of 163 Root Nodule Bacteria
journal, November 2015

  • Seshadri, Rekha; Reeve, Wayne G.; Ardley, Julie K.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep16825

Theczc operon ofAlcaligenes eutrophus CH34: from resistance mechanism to the removal of heavy metals
journal, February 1995

  • Diels, Ludo; Dong, Qinghan; Lelie, Daniël
  • Journal of Industrial Microbiology, Vol. 14, Issue 2
  • DOI: 10.1007/BF01569896

MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013

  • Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
  • Molecular Biology and Evolution, Vol. 30, Issue 12
  • DOI: 10.1093/molbev/mst197

Legume Symbiotic Nitrogen Fixation by  -Proteobacteria Is Widespread in Nature
journal, December 2003


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0

ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH-induced copper toxicity
journal, February 2002


IMG ER: a system for microbial genome annotation expert review and curation
journal, June 2009


tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997


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