{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T05:09:22Z","timestamp":1780463362914,"version":"3.54.1"},"reference-count":51,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2018,11,23]],"date-time":"2018-11-23T00:00:00Z","timestamp":1542931200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31770123"],"award-info":[{"award-number":["31770123"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001711","name":"Schweizerischer Nationalfonds zur F\u00f6rderung der Wissenschaftlichen Forschung","doi-asserted-by":"publisher","award":["31003A_175638"],"award-info":[{"award-number":["31003A_175638"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Heavy metals (HMs) are compounds that can be hazardous and impair growth of living organisms. Bacteria have evolved the capability not only to cope with heavy metals but also to detoxify polluted environments. Three heavy metal-resistant strains of Mucilaginibacer rubeus and one of Mucilaginibacter kameinonensis were isolated from the gold\/copper Zijin mining site, Longyan, Fujian, China. These strains were shown to exhibit high resistance to heavy metals with minimal inhibitory concentration reaching up to 3.5 mM Cu(II), 21 mM Zn(II), 1.2 mM Cd(II), and 10.0 mM As(III). Genomes of the four strains were sequenced by Illumina. Sequence analyses revealed the presence of a high abundance of heavy metal resistance (HMR) determinants. One of the strain, M. rubeus P2, carried genes encoding 6 putative PIB-1-ATPase, 5 putative PIB-3-ATPase, 4 putative Zn(II)\/Cd(II) PIB-4 type ATPase, and 16 putative resistance-nodulation-division (RND)-type metal transporter systems. Moreover, the four genomes contained a high abundance of genes coding for putative metal binding chaperones. Analysis of the close vicinity of these HMR determinants uncovered the presence of clusters of genes potentially associated with mobile genetic elements. These loci included genes coding for tyrosine recombinases (integrases) and subunits of mating pore (type 4 secretion system), respectively allowing integration\/excision and conjugative transfer of numerous genomic islands. Further in silico analyses revealed that their genetic organization and gene products resemble the Bacteroides integrative and conjugative element CTnDOT. These results highlight the pivotal role of genomic islands in the acquisition and dissemination of adaptive traits, allowing for rapid adaption of bacteria and colonization of hostile environments.<\/jats:p>","DOI":"10.3390\/genes9120573","type":"journal-article","created":{"date-parts":[[2018,11,23]],"date-time":"2018-11-23T12:20:28Z","timestamp":1542975628000},"page":"573","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Genomic Islands Confer Heavy Metal Resistance in Mucilaginibacter kameinonensis and Mucilaginibacter rubeus Isolated from a Gold\/Copper Mine"],"prefix":"10.3390","volume":"9","author":[{"given":"Yuan Ping","family":"Li","sequence":"first","affiliation":[{"name":"Institute of Environmental Microbiology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Carraro","sequence":"additional","affiliation":[{"name":"Department of Fundamental Microbiology, University of Lausanne, Lausanne 1015, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nan","family":"Yang","sequence":"additional","affiliation":[{"name":"Institute of Environmental Microbiology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bixiu","family":"Liu","sequence":"additional","affiliation":[{"name":"Institute of Environmental Microbiology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xian","family":"Xia","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renwei","family":"Feng","sequence":"additional","affiliation":[{"name":"Institute of Environmental Microbiology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Quaiser","family":"Saquib","sequence":"additional","affiliation":[{"name":"Zoology Department, College of Sciences, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hend A","family":"Al-Wathnani","sequence":"additional","affiliation":[{"name":"Department of Botany &amp; Microbiology, College of Sciences, P.O. Box 2455, Riyadh 11451, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan Roelof","family":"Van der Meer","sequence":"additional","affiliation":[{"name":"Department of Fundamental Microbiology, University of Lausanne, Lausanne 1015, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher","family":"Rensing","sequence":"additional","affiliation":[{"name":"Institute of Environmental Microbiology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academic of Sciences, 361021 Xiamen, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,11,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1038\/nrmicro.2017.15","article-title":"Metal homeostasis and resistance in bacteria","volume":"15","author":"Chandrangsu","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1007\/s00248-006-9192-z","article-title":"Effects of experimental lead pollution on the microbial communities associated with Sphagnum fallax (Bryophyta)","volume":"54","author":"Gilbert","year":"2007","journal-title":"Microb. Ecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1016\/j.tim.2016.03.004","article-title":"Microbial ecology and evolution in the acid mine drainage model system","volume":"24","author":"Huang","year":"2016","journal-title":"Trends Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/S0168-6445(03)00048-2","article-title":"Efflux-mediated heavy metal resistance in prokaryotes","volume":"27","author":"Nies","year":"2003","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1039\/C5MT00320B","article-title":"The biological chemistry of the transition metal \u201ctransportome\u201d of Cupriavidus metallidurans","volume":"8","author":"Nies","year":"2016","journal-title":"Metallomics"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"96","DOI":"10.4161\/mge.19963","article-title":"Distribution of horizontally transferred heavy metal resistance operons in recent outbreak bacteria","volume":"2","author":"Reva","year":"2012","journal-title":"Mob. Genet. Elem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1046\/j.1365-2958.2002.03014.x","article-title":"Bacterial conjugation: A two-step mechanism for DNA transport","volume":"45","author":"Llosa","year":"2010","journal-title":"Mol. Microbiol."},{"key":"ref_8","first-page":"81","article-title":"Towards an integrated model of bacterial conjugation","volume":"39","author":"Arechaga","year":"2014","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"7417","DOI":"10.1128\/JB.00375-07","article-title":"Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals","volume":"189","author":"Monchy","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/S0168-6445(03)00045-7","article-title":"Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: Towards a catalogue of metal-responsive genes","volume":"27","author":"Mergeay","year":"2010","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.plasmid.2018.07.003","article-title":"A plasmid-encoded mobile genetic element from Pseudomonas aeruginosa that confers heavy metal resistance and virulence","volume":"98","year":"2018","journal-title":"Plasmid"},{"key":"ref_12","first-page":"96","article-title":"Mainstreams of horizontal gene exchange in enterobacteria: Consideration of the outbreak of enterohemorrhagic E","volume":"2","author":"Bezuidt","year":"2012","journal-title":"coli O104:H4 in Germany in 2011. PLoS ONE"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5169","DOI":"10.1093\/nar\/29.24.5169","article-title":"The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa","volume":"29","author":"Schneiker","year":"2001","journal-title":"Nucl. Acids Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.plasmid.2004.06.006","article-title":"The complete nucleotide sequence of the resistance plasmid R478: Defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics","volume":"52","author":"Gilmour","year":"2004","journal-title":"Plasmid"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3477","DOI":"10.1099\/mic.0.29056-0","article-title":"Plasmid pBP136 from Bordetella pertussis represents an ancestral form of IncP-1\u03b2 plasmids without accessory mobile elements","volume":"152","author":"Kamachi","year":"2006","journal-title":"Microbiology"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Guglielmini, J., Quintais, L., Garcill\u00e1n-Barcia, M.P., De la Cruz, F., and Rocha, E.P.C. (2011). The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1002222"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1080\/2159256X.2015.1102796","article-title":"The dualistic nature of integrative and conjugative elements","volume":"5","author":"Carraro","year":"2015","journal-title":"Mob. Genet. Elem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/2159256X.2017.1304193","article-title":"Mobilizable genomic islands, different strategies for the dissemination of multidrug resistance and other adaptive traits","volume":"7","author":"Carraro","year":"2017","journal-title":"Mob. Genet. Elem."},{"key":"ref_19","first-page":"811","article-title":"Evolution of a heavy metal homeostasis\/resistance island reflects increasing copper stress in enterobacteria","volume":"8","author":"Staehlin","year":"2016","journal-title":"Genome Boil. Evol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1128\/AEM.01189-17","article-title":"The arsenic resistance Listeria genomic island LGI2 exhibits sequence and integration site diversity and propensity for three Listeria monocytogenes clones with enhanced virulence","volume":"83","author":"Lee","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Al-Jabri, Z., Zamudio, R., Horvath-Papp, E., Ralph, J., Al-Muharrami, Z., Rajakumar, K., and Oggioni, M. (2018). Integrase-controlled excision of metal-resistance genomic islands in Acinetobacter baumannii. Genes, 9.","DOI":"10.3390\/genes9070366"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1128\/AAC.01229-06","article-title":"SGI1-K, a variant of the SGI1 genomic island carrying a mercury resistance region, in Salmonella enterica serovar Kentucky","volume":"51","author":"Levings","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Carraro, N., Matteau, D., Luo, P., Rodrigue, S., and Burrus, V. (2014). The master activator of IncA\/C conjugative plasmids stimulates genomic islands and multidrug resistance dissemination. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004714"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Carraro, N., Durand, R., Rivard, N., Anquetil, C., Barrette, C., Humbert, M., and Burrus, V. (2017). Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation. PLoS Genet., 13.","DOI":"10.1371\/journal.pgen.1006705"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.plasmid.2008.08.001","article-title":"Revised nomenclature for transposable genetic elements","volume":"60","author":"Roberts","year":"2008","journal-title":"Plasmid"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1021\/bi00596a021","article-title":"Primary structure of protein L19 from the large subunit of Escherichia coli ribosomes","volume":"17","author":"Brosius","year":"1978","journal-title":"Biochemistry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2259","DOI":"10.1099\/ijs.0.64915-0","article-title":"EzTaxon: A web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences","volume":"57","author":"Chun","year":"2007","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2725","DOI":"10.1093\/molbev\/mst197","article-title":"MEGA6: Molecular evolutionary genetics analysis version 6.0","volume":"30","author":"Tamura","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/BF01731581","article-title":"A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences","volume":"16","author":"Kimura","year":"1980","journal-title":"J. Mol. Evol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"783","DOI":"10.2307\/2408678","article-title":"Confidence limit on phylogenies: An approach using the bootstrap","volume":"39","author":"Felsenstein","year":"1985","journal-title":"Evolution"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"Muscle: Multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucl. Acids Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1093\/bioinformatics\/8.3.275","article-title":"The rapid generation of mutation data matrices from protein sequences","volume":"8","author":"Jones","year":"1992","journal-title":"Bioinformatics"},{"key":"ref_33","unstructured":"Tang, J. (2017). Identification and Genome Analysis of Mucilaginibacter pedocola sp. nov. [Ph.D. Thesis, Huazhong Agriculture University]."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1007\/s12275-017-7180-2","article-title":"Mucilaginibacter hankyongensis, sp. nov. isolated from soil of ginseng field Baekdu mountain","volume":"55","author":"Liu","year":"2017","journal-title":"J. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00284-017-1329-4","article-title":"Mucilaginibacter ginsenosidivorans, sp. nov. isolated from soil of ginseng field","volume":"74","author":"Kim","year":"2017","journal-title":"Curr. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4033","DOI":"10.1099\/ijsem.0.001306","article-title":"Mucilaginibacter pedocola sp. nov. isolated from a heavy-metal-contaminated paddy field","volume":"66","author":"Tang","year":"2016","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2108","DOI":"10.1073\/pnas.1721783115","article-title":"Cu+-specific CopB transporter: Revising P1B-type ATPase classification","volume":"115","author":"Purohit","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1128\/jb.162.1.328-334.1985","article-title":"Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals","volume":"162","author":"Mergeay","year":"1985","journal-title":"J. Bacteriol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Janssen, P.J., Van Houdt, R., Moors, H., Monsieurs, P., Morin, N., Michaux, A., Benotmane, M.A., Leys, N., Vallaeys, T., and Lapidus, A. (2010). The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010433"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/ecosalplus.esp-0020-2015","article-title":"The mosaic type IV secretion systems","volume":"7","author":"Christie","year":"2016","journal-title":"EcoSal Plus"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"5715","DOI":"10.1093\/nar\/gku194","article-title":"Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion","volume":"42","author":"Guglielmini","year":"2014","journal-title":"Nucl. Acids Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1006\/plas.2001.1552","article-title":"Mobile elements as a combination of functional modules","volume":"47","author":"Toussaint","year":"2002","journal-title":"Plasmid"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1146\/annurev-genet-112414-055018","article-title":"Integrative and conjugative elements (ICEs): What they do and how they work","volume":"49","author":"Johnson","year":"2015","journal-title":"Annu. Rev. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3601","DOI":"10.1128\/jb.178.12.3601-3607.1996","article-title":"NBU1, a mobilizable site-specific integrated element from Bacteroides spp. can integrate non-specifically in Escherichia coli","volume":"178","author":"Shoemaker","year":"1996","journal-title":"J. Bacteriol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1128\/JB.01015-10","article-title":"Characterization of the Bacteroides CTnDOT regulatory protein RteC","volume":"193","author":"Park","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1046\/j.1365-2958.2001.02519.x","article-title":"Identification of genes required for excision of CTnDOT, a Bacteroides conjugative transposon","volume":"41","author":"Cheng","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1093\/femsre\/fux008","article-title":"The hidden life of integrative and conjugative elements","volume":"41","author":"Delavat","year":"2017","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Carraro, N., and Burrus, V. (2014). Biology of three ICE families: SXT\/R391, ICEBs1, and ICESt1\/ICESt3. Microbiol. Spectr., 2.","DOI":"10.1128\/microbiolspec.MDNA3-0008-2014"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Wood, M.M., and Gardner, J.F. (2015). The integration and excision of CTnDOT. Microbiol. Spectr., 3.","DOI":"10.1128\/microbiolspec.MDNA3-0020-2014"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2349","DOI":"10.1099\/ijs.0.65100-0","article-title":"Mucilaginibacter paludis gen. nov. sp. nov. and Mucilaginibacter gracilis sp. nov. pectin-, xylan- and laminarin-degrading members of the family Sphingobacteriaceae from acidic Sphagnum peat bog","volume":"57","author":"Pankratov","year":"2007","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2451","DOI":"10.1099\/ijs.0.018713-0","article-title":"Mucilaginibacter gossypii sp. nov. and Mucilaginibacter gossypiicola sp. nov. plant-growth-promoting bacteria isolated from cotton rhizosphere soils","volume":"60","author":"Madhaiyan","year":"2010","journal-title":"Int. J. Syst. Evol. Microbiol."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/12\/573\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:31:49Z","timestamp":1760196709000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/12\/573"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,11,23]]},"references-count":51,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["genes9120573"],"URL":"https:\/\/doi.org\/10.3390\/genes9120573","relation":{"has-preprint":[{"id-type":"doi","id":"10.20944\/preprints201810.0505.v1","asserted-by":"object"}]},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,11,23]]}}}