Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to Zinc and Cadmium exposure

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Maynaud, Géraldine ^a   Brunel, Brigitte ^b   Mornico, Damien ^c   Durot, Maxime ^c   Severac, Dany ^d   Dubois, Emeric ^d   Navarro, Elisabeth ^e   Cleyet Marel, Jean Claude ^a   Le Quéré, Antoine ^e  

^a CEMAGREF   (France)

^b MONTPELLIER SUPAGRO   (France)

^c CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^e INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Cadmium; Comparative genomics and transcriptomics; Mesorhizobium; Metal tolerant rhizobia; RNAseq; Zinc; znuABC

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CADMIUM; ZINC; ABC TRANSPORTER; ANTIINFECTIVE AGENT; TRANSCRIPTOME;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE MAPPING; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CODE; GENOME ANALYSIS; LONG TERM EXPOSURE; MESORHIZOBIUM; MESORHIZOBIUM METALLIDURANS; MESORHIZOBIUM TIANSHANENSE; METAL TOLERANCE; NONHUMAN; RNA SEQUENCE; SYMBIONT; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UPREGULATION; BACTERIAL GENE; CHROMOSOME MAP; DRUG EFFECTS; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; SYMBIOSIS; TRANSPORT AT THE CELLULAR LEVEL;

ANTHYLLIS VULNERARIA; MESORHIZOBIUM;

ADENOSINE TRIPHOSPHATASES; ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CADMIUM; CHROMOSOME MAPPING; CONSERVED SEQUENCE; GENES, BACTERIAL; GENOMICS; MESORHIZOBIUM; MOLECULAR SEQUENCE ANNOTATION; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; SYMBIOSIS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; ZINC;

EID: 84876795645     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-292     Document Type: Article

References (60)

1. Kampa M, Castanas E. Human health effects of air pollution. Environ Pollut 2008, 151(2):362-367. 10.1016/j.envpol.2007.06.012, 17646040.
2. Nwuche CO, Ugoji EO. Effects of heavy metal pollution on the soil microbial activity. Int J Environ Sci Te 2008, 5(3):409-414.
3. Ghosh M, Singh SP. A Review on Phytoremediation of Heavy Metals and Utilization of It's by Products. Asian J Energy Environ 2005, 6(4):18.
4. Frérot H, Lefebvre C, Gruber W, Collin C, Dos Santos A, Escarre J. Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant Soil 2006, 282(1-2):53-65.
5. Mahieu S, Frerot H, Vidal C, Galiana A, Heulin K, Maure L, Brunel B, Lefebvre C, Escarre J, Cleyet-Marel JC. Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn. Pb and Cd. Plant Soil 2011, 342(1-2):405-417.
6. Escarre J, Lefebvre C, Raboyeau S, Dossantos A, Gruber W, Marel JCC, Frérot H, Noret N, Mahieu S, Collin C. Heavy Metal Concentration Survey in Soils and Plants of the Les Malines Mining District (Southern France): Implications for Soil Restoration. Wat Air Soil Pollut 2011, 216(1-4):485-504.
7. Vidal C, Chantreuil C, Berge O, Maure L, Escarre J, Bena G, Brunel B, Cleyet-Marel JC. Mesorhizobium metallidurans sp nov., a metal-resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France. Int J Syst Evol Microbiol 2009, 59:850-855. 10.1099/ijs.0.003327-0, 19329619.
8. Nies DH. Microbial heavy-metal resistance. Appl Microbiol Biotech 1999, 51(6):730-750.
9. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 2003, 27(2-3):313-339.
10. Ma Z, Jacobsen FE, Giedroc DP. Coordination Chemistry of Bacterial Metal Transport and Sensing. Chem Rev 2009, 109(10):4644-4681. 10.1021/cr900077w, 2783614, 19788177.
11. Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A. The Complete Genome Sequence of Cupriavidus metallidurans Strain CH34, a Master Survivalist in Harsh and Anthropogenic Environments. PLoS One 2010, 5(5):e10433. 10.1371/journal.pone.0010433, 2864759, 20463976.
12. Monsieurs P, Moors H, Van Houdt R, Janssen PJ, Janssen A, Coninx I, Mergeay M, Leys N. Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network. BioMetals 2011, 24(6):1133-1151. 10.1007/s10534-011-9473-y, 21706166.
13. Vallenet D, Engelen S, Mornico D, Cruveiller S, Fleury L, Lajus A, Rouy Z, Roche D, Salvignol G, Scarpelli C. MicroScope: a platform for microbial genome annotation and comparative genomics. Database (Oxford) 2009, 2009:bap021.
14. Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, van der Lelie D, Mergeay M. Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 2007, 189(20):7417-7425. 10.1128/JB.00375-07, 2168447, 17675385.
15. MicroScope web interface RNAseq projects http://www.genoscope.cns.fr/agc/microscope/expdata/rnaseqProjects.php.
16. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.
17. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met 1995, 57(1):289-300.
18. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001, 29(1):22-28. 10.1093/nar/29.1.22, 29819, 11125040.
19. Pereira SI, Lima AI, Figueira EM. Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microb Ecol 2006, 52(2):176-186. 10.1007/s00248-006-9057-5, 16897308.
20. Wang AY, Crowley DE. Global gene expression responses to cadmium toxicity in Escherichia coli. J Bacteriol 2005, 187(9):3259-3266. 10.1128/JB.187.9.3259-3266.2005, 1082819, 15838054.
21. Kawaharada Y, Kiyota H, Eda S, Minamisawa K, Mitsui H. Identification of the Mesorhizobium loti gene responsible for glycerophosphorylation of periplasmic cyclic beta-1,2-glucans. FEMS Microbiol Lett 2010, 302(2):131-137. 10.1111/j.1574-6968.2009.01843.x, 19951365.
22. Taghavi S, Lesaulnier C, Monchy S, Wattiez R, Mergeay M, van der Lelie D. Lead(II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions. Antonie Van Leeuwenhoek 2009, 96(2):171-182. 10.1007/s10482-008-9289-0, 18953667.
23. Aiking H, Kok K,. van Heerikhuizen H, van 't Riet J Adaptation to Cadmium by Klebsiella aerogenes Growing in Continuous Culture Proceeds Mainly via Formation of Cadmium Sulfide. Appl Environ Microbiol 1982, 44(4):938-944. 242120, 16346119, van Heerikhuizen H, van 't Riet J.
24. McEntee JD, Woodrow JR, Quirk AV. Investigation of cadmium resistance in an Alcaligenes sp. Appl Environ Microbiol 1986, 51(3):515-520. 238911, 3963810.
25. Macaskie LE, Bonthrone KM, Yong P, Goddard DT. Enzymically mediated bioprecipitation of uranium by a Citrobacter sp.: a concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation. Microbiology-Uk 2000, 146:1855-1867.
26. Zeller T, Klug G. Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes. Naturwissenschaften 2006, 93(6):259-266. 10.1007/s00114-006-0106-1, 16555095.
27. Li XK, Krumholz LR. Thioredoxin Is Involved in U(VI) and Cr(VI) Reduction in Desulfovibrio desulfuricans G20. J Bacteriol 2009, 191(15):4924-4933. 10.1128/JB.00197-09, 2715717, 19482922.
28. Slaveykova VI, Parthasarathy N, Dedieu K, Toescher D. Role of extracellular compounds in Cd-sequestration relative to Cd uptake by bacterium Sinorhizobium meliloti. Environ Pollut 2010, 158(8):2561-2565. 10.1016/j.envpol.2010.05.016, 20541857.
29. Yamamoto K, Ishihama A. Transcriptional response of Escherichia coli to external zinc. J Bacteriol 2005, 187(18):6333-6340. 10.1128/JB.187.18.6333-6340.2005, 1236622, 16159766.
30. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ. Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol Microbiol 2002, 45(5):1421-1432. 10.1046/j.1365-2958.2002.03109.x, 12207707.
31. Grass G, Fan B, Rosen BP, Franke S, Nies DH, Rensing C. ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli. J Bacteriol 2001, 183(15):4664-4667. 10.1128/JB.183.15.4664-4667.2001, 95364, 11443104.
32. Anton A, Grosse C, Reissmann J, Pribyl T, Nies DH. CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J Bacteriol 1999, 181(22):6876-6881. 94160, 10559151.
33. Paulsen IT, Saier MH. A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 1997, 156(2):99-103. 10.1007/s002329900192, 9075641.
34. Perreten V, Schwarz FV, Teuber M, Levy SB. Mdt(A), a new efflux protein conferring multiple antibiotic resistance in Lactococcus lactis and Escherichia coli. Antimicrob Agents Chemotherapy 2001, 45(4):1109-1114.
35. Nishino K, Nikaido E, Yamaguchi A. Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar typhimurium. J Bacteriol 2007, 189(24):9066-9075. 10.1128/JB.01045-07, 2168627, 17933888.
36. Lee LJ, Barrett JA, Poole RK. Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J Bacteriol 2005, 187(3):1124-1134. 10.1128/JB.187.3.1124-1134.2005, 545701, 15659689.
37. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. Co-selection of antibiotic and metal resistance. Trends Microbiol 2006, 14(4):176-182. 10.1016/j.tim.2006.02.006, 16537105.
38. Arguello JM. Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J Membr Biol 2003, 195(2):93-108. 10.1007/s00232-003-2048-2, 14692449.
39. Rossbach S, Mai DJ, Carter EL, Sauviac L, Capela D, Bruand C, de Bruijn FJ. Response of Sinorhizobium meliloti to elevated concentrations of cadmium and zinc. Appl Environ Microbiol 2008, 74(13):4218-4221. 10.1128/AEM.02244-07, 2446505, 18469129.
40. Rensing C, Mitra B, Rosen BP. The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Natl Acad Sci USA 1997, 94(26):14326-14331. 10.1073/pnas.94.26.14326, 24962, 9405611.
41. Nucifora G, Chu L, Misra TK, Silver S. Cadmium Resistance from Staphylococcus-Aureus Plasmid Pi258 CadA Gene Results from a Cadmium-Efflux ATPase. Proc Natl Acad Sci USA 1989, 86(10):3544-3548. 10.1073/pnas.86.10.3544, 287174, 2524829.
42. Fabianek RA, Hennecke H, Thony-Meyer L. Periplasmic protein thiol: disulfide oxidoreductases of Escherichia coli. FEMS Microbiol Rev 2000, 24(3):303-316. 10.1111/j.1574-6976.2000.tb00544.x, 10841975.
43. Fong ST, Camakaris J, Lee BTO. Molecular-Genetics of a Chromosomal Locus Involved in Copper Tolerance in Escherichia coli K-12. Mol Microbiol 1995, 15(6):1127-1137. 10.1111/j.1365-2958.1995.tb02286.x, 7623666.
44. Patzer SI, Hantke K. The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 1998, 28(6):1199-1210. 10.1046/j.1365-2958.1998.00883.x, 9680209.
45. Patzer SI, Hantke K. The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J Biol Chem 2000, 275(32):24321-24332. 10.1074/jbc.M001775200, 10816566.
46. Panina EM, Mironov AA, Gelfand MS. Comparative genomics of bacterial zinc regulons: Enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci USA 2003, 100(17):9912-9917. 10.1073/pnas.1733691100, 187884, 12904577.
47. Petrarca P, Ammendola S, Pasquali P, Battistoni A. The Zur-Regulated ZinT Protein Is an Auxiliary Component of the High-Affinity ZnuABC Zinc Transporter That Facilitates Metal Recruitment during Severe Zinc Shortage. J Bacteriol 2010, 192(6):1553-1564. 10.1128/JB.01310-09, 2832539, 20097857.
48. Gabbianelli R, Scotti R, Ammendola S, Petrarca P, Nicolini L, Battistoni A. Role of ZnuABC and ZinT in Escherichia coli O157:H7 zinc acquisition and interaction with epithelial cells. BMC Microbiol 2011, 11:36. 10.1186/1471-2180-11-36, 3053223, 21338480.
49. Miller WG, Leveau JHJ, Lindow SE. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microb Interact 2000, 13(11):1243-1250.
50. Beringer JE. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 1974, 84(1):188-198. 10.1099/00221287-84-1-188, 4612098.
51. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual 1989, New York: Cold Spring Harbour Laboratory Press, 2.
52. Chen WP, Kuo TT. A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Nucleic Acids Res 1993, 21(9):2260-2260. 10.1093/nar/21.9.2260, 309503, 8502576.
53. Genome Browser MaGe interface https://www.genoscope.cns.fr/agc/microscope/mage/viewer.php.
54. MicroScope collaborative projects https://www.genoscope.cns.fr/agc/microscope/about/collabprojects.php?P_id=3.
55. Ning Z, Cox AJ, Mullikin JC. SSAHA: a fast search method for large DNA databases. Genome Res 2001, 11(10):1725-1729. 10.1101/gr.194201, 311141, 11591649.
56. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26(6):841-842. 10.1093/bioinformatics/btq033, 2832824, 20110278.
57. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45. 10.1093/nar/29.9.e45, 55695, 11328886.
58. Hayashi M, Maeda Y, Hashimoto Y, Murooka Y. Efficient transformation of Mesorhizobium huakuii subsp. rengei and Rhizobium species. J Biosci Bioeng 2000, 89(6):550-553. 10.1016/S1389-1723(00)80055-9, 16232796.
59. Durfee T, Nelson R, Baldwin S, Plunkett G, Burland V, Mau B, Petrosino JF, Qin X, Muzny DM, Ayele M. The Complete Genome Sequence of Escherichia coli DH10B: Insights into the Biology of a Laboratory Workhorse. J Bacteriol 2008, 190(7):2597-2606. 10.1128/JB.01695-07, 2293198, 18245285.
60. Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gilli M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 1997, 47(3):895-898.