Comparative genome analyses uncovered the cadmium resistance mechanism of enterobacter cloacae.
Cadmium resistance
Enterobacter cloacae
Genome comparative analysis
Journal
International microbiology : the official journal of the Spanish Society for Microbiology
ISSN: 1618-1905
Titre abrégé: Int Microbiol
Pays: Switzerland
ID NLM: 9816585
Informations de publication
Date de publication:
Jan 2023
Jan 2023
Historique:
received:
01
05
2022
accepted:
06
09
2022
revised:
29
08
2022
pubmed:
23
9
2022
medline:
6
1
2023
entrez:
22
9
2022
Statut:
ppublish
Résumé
Cadmium (Cd) can be transported into plants from polluted soils and may cause animal and human diseases through food chains, which requires the development of highly efficient methods for soil Cd remediation. Although we isolated an Enterobacter cloacae strain Cu6 with Cd resistance, this strain cannot be used for soil Cd remediation due to its lower resistance. Here, we domesticated Cu6 and obtained a highly Cd-resistant strain, LPY6, and found that this strain can attenuate the toxic effects of Cd on wheat seedling growth. We deciphered the high Cd-resistance mechanism of LPY6 by genome comparative and genetic analysis. Compared with Cu6, 75 genes were mutated in LPY6. Thirty-four of these genes were deleted, and 41 had single nucleotide polymorphisms (SNPs). Most of these mutated proteins are involved in basic metabolism, substrate transport, stress response and formate and hydrogen metabolism. RNA quantitative analysis and promoter activity assays showed that the transcription or mRNA levels of two operons (cadA and norVW) in these mutated genes were regulated by Cd, zinc (Zn) or lead (Pb) ions, suggesting that these two operons might be required for Cd, Zn or Pb resistance. Expression of cadA and norVW operons in LPY6 partially recovered Cd susceptibility, demonstrating that CadA and NorVW are involved in Cd resistance in E. cloacae. Our findings illustrate that E. cloacae acquires Cd resistance through different pathways and lay a foundation for developing highly efficient methods for soil Cd remediation.
Identifiants
pubmed: 36136279
doi: 10.1007/s10123-022-00276-3
pii: 10.1007/s10123-022-00276-3
doi:
Substances chimiques
Cadmium
00BH33GNGH
Lead
2P299V784P
Soil
0
Zinc
J41CSQ7QDS
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
99-108Subventions
Organisme : Natural Science Foundation of Hainan Province
ID : 2019RC063
Organisme : Construction of World First Class Discipline of Hainan University
ID : RZZX201903
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Bagot D, Lebeau T, Jezequel K (2006) Microorganisms for remediation of cadmium-contaminated soils. Environ Chem Lett 4:207–211. https://doi.org/10.1007/s10311-006-0047-0
doi: 10.1007/s10311-006-0047-0
Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P (2007) CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform 8:209–209. https://doi.org/10.1186/1471-2105-8-209
doi: 10.1186/1471-2105-8-209
Cali DS, Kim JS, Ghose S, Alkan C, Mutlu O (2019) Nanopore sequencing technology and tools for genome assembly: computational analysis of the current state, bottlenecks and future directions. Brief Bioinform 20:1542–1559. https://doi.org/10.1093/bib/bby017
doi: 10.1093/bib/bby017
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421. https://doi.org/10.1186/1471-2105-10-421
doi: 10.1186/1471-2105-10-421
Chuanboon K, Na Nakorn P, Pannengpetch S, Laengsri V, Nuchnoi P, Isarankura-Na-Ayudhya C, Isarankura-Na-Ayudhya P (2019) Proteomics and bioinformatics analysis reveal potential roles of cadmium-binding proteins in cadmium tolerance and accumulation of Enterobacter cloacae. PeerJ 7:e6904. https://doi.org/10.7717/peerj.6904
doi: 10.7717/peerj.6904
Engelhardt BE, Jordan MI, Srouji JR, Brenner SE (2011) Genome-scale phylogenetic function annotation of large and diverse protein families. Genome Res 21:1969–1980. https://doi.org/10.1101/gr.104687.109
doi: 10.1101/gr.104687.109
Gardner AM, Gardner PR (2002) Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J Biol Chem 277:8166–8171. https://doi.org/10.1074/jbc.M110470200
doi: 10.1074/jbc.M110470200
Haq R, Zaidi SK, Shakoori AR (1999) Cadmium resistant Enterobacter cloacae and Klebsiella sp. isolated from industrial effluents and their possible role in cadmium detoxification. World J Microb and Biotech 15:283–290. https://doi.org/10.1023/A:1008986727896
doi: 10.1023/A:1008986727896
Hatori Y, Lewis D, Toyoshima C, Inesi G (2009) Reaction cycle of Thermotoga maritima copper ATPase and conformational characterization of catalytically deficient mutants. Biochemistry 48:4871–4880. https://doi.org/10.1021/bi900338n
doi: 10.1021/bi900338n
Hou ZJ, Narindrasorasak S, Bhushan B, Sarkar B, Mitra B (2001) Functional analysis of chimeric proteins of the Wilson Cu(I)-ATPase (ATP7B) and ZntA, a Pb(II)/Zn(II)/Cd(II)-ATPase from Escherichia coli. J Biol Chem 276:40858–40863. https://doi.org/10.1074/jbc.M107455200
doi: 10.1074/jbc.M107455200
Hudson CM, Lau BY, Williams KP (2015) Islander: a database of precisely mapped genomic islands in tRNA and tmRNA genes. Nucleic Acids Res 43:D48–D53. https://doi.org/10.1093/nar/gku1072
doi: 10.1093/nar/gku1072
Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. Bmc Bioinform 11. https://doi.org/10.1186/1471-2105-11-119
Kolmogorov M, Yuan J, Lin Y, Pevzner P (2018) Assembly of Long Error-Prone Reads Using Repeat Graphs 22nd Annual International Conference on Research in Computational Molecular Biology (RECOMB) (Lecture Notes in Bioinformatics), Sorbonne Univ, Pierre Marie Curie Campus, Paris, FRANCE, pp. 261–262.
Kurt-Gur G, Demirci H, Sunulu A, Ordu E (2018) Stress response of NAD(+)-dependent formate dehydrogenase in Gossypium hirsutum L. grown under copper toxicity. Environ Sci Pollut Res Int 25:31679–31690. https://doi.org/10.1007/s11356-018-3145-1
doi: 10.1007/s11356-018-3145-1
Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108. https://doi.org/10.1093/nar/gkm160
doi: 10.1093/nar/gkm160
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
doi: 10.1093/bioinformatics/btp324
Li C, Liu S, Liu P, Wang Y, Xu C, Tao J, He C (2018) The YebN Leader RNA Acts as a Mn(2+) Sensor Required for the Interaction of Xanthomonas oryzae and Rice. Mol Plant Microbe Interact 31:932–939. https://doi.org/10.1094/MPMI-02-18-0043-R
doi: 10.1094/MPMI-02-18-0043-R
Liu S, Liu P, Xu Y, Long Y, Niu X, Li C, Chen Y, Tao J (2019) Isolation and Identification of a Multiple Resistant Bacterium to Heavy Metals. J Trop Biol 10:41–46. https://doi.org/10.15886/j.cnki.rdswxb.2019.01.007
doi: 10.15886/j.cnki.rdswxb.2019.01.007
Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57. https://doi.org/10.1093/nar/gkw413
doi: 10.1093/nar/gkw413
Lu F-Z, Li Q-Q, He H-Y, Qin Y-R, Meng L-Z (2016) Isolation and characterization of cadmium resistance fungus. Environ Engine 5:64–67. https://doi.org/10.13205/j.hjgc.201604014
doi: 10.13205/j.hjgc.201604014
Maehara Y, Tsujitani S, Saeki H, Oki E, Yoshinaga K, Emi Y, Morita M, Kohnoe S, Kakeji Y, Yano T, Baba H (2012) Biological mechanism and clinical effect of protein-bound polysaccharide K (KRESTIN((R))): review of development and future perspectives. Surg Today 42:8–28. https://doi.org/10.1007/s00595-011-0075-7
doi: 10.1007/s00595-011-0075-7
McDowall JS, Murphy BJ, Haumann M, Palmer T, Armstrong FA, Sargent F (2014) Bacterial formate hydrogenlyase complex. Proc Natl Acad Sci U S A 111:E3948-3956. https://doi.org/10.1073/pnas.1407927111
doi: 10.1073/pnas.1407927111
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935. https://doi.org/10.1093/bioinformatics/btt509
doi: 10.1093/bioinformatics/btt509
Okkeri J, Haltia T (1999) Expression and mutagenesis of ZntA, a zinc-transporting P-type ATPase from Escherichia coli. Biochemistry 38:14109–14116. https://doi.org/10.1021/bi9913956
doi: 10.1021/bi9913956
Sun R, Wang L, Huang R, Huang F, Gan D, Wang J, Guan R, Han W, Qu J, Yan L, Zhang Y (2020) Cadmium resistance mechanisms of a functional strain Enterobacter sp DNB-S2 isolated from black soil in Northeast China. Environ Pollut 263:114612. https://doi.org/10.1016/j.envpol.2020.114612
doi: 10.1016/j.envpol.2020.114612
Thomas SC, Alhasawi A, Auger C, Omri A, Appanna VD (2016) The role of formate in combatting oxidative stress. Antonie Van Leeuwenhoek 109:263–271. https://doi.org/10.1007/s10482-015-0629-6
doi: 10.1007/s10482-015-0629-6
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM (2014) Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. Plos One 9. https://doi.org/10.1371/journal.pone.0112963
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49. https://doi.org/10.1093/nar/gkr1293
doi: 10.1093/nar/gkr1293
Xiao Y, Xiao C, Zhao F (2019) Long-term adaptive evolution of Shewanella oneidensis MR-1 for establishment of high concentration Cr(VI) tolerance. Front Environ Sci & Engin 14:3. https://doi.org/10.1007/s11783-019-1182-8
doi: 10.1007/s11783-019-1182-8
Xie Y, Bu H, Feng Q, Wassie M, Amee M, Jiang Y, Bi Y, Hu L, Chen L (2021) Identification of Cd-resistant microorganisms from heavy metal-contaminated soil and its potential in promoting the growth and Cd accumulation of bermudagrass. Environ Res 200:111730. https://doi.org/10.1016/j.envres.2021.111730
doi: 10.1016/j.envres.2021.111730
Xu C, He S, Liu Y, Zhang W, Lu D (2017) Bioadsorption and biostabilization of cadmium by Enterobacter cloacae TU. Chemosphere 173:622–629. https://doi.org/10.1016/j.chemosphere.2017.01.005
doi: 10.1016/j.chemosphere.2017.01.005
Yu X, Ding Z, Ji Y, Zhao J, Liu X, Tian J, Wu N, Fan Y (2020) An operon consisting of a P-type ATPase gene and a transcriptional regulator gene responsible for cadmium resistances in Bacillus vietamensis 151–6 and Bacillus marisflavi 151–25. BMC Microbiol 20:18. https://doi.org/10.1186/s12866-020-1705-2
doi: 10.1186/s12866-020-1705-2
Zielazinski EL, Cutsail GE 3rd, Hoffman BM, Stemmler TL, Rosenzweig AC (2012) Characterization of a cobalt-specific P(1B)-ATPase. Biochemistry 51:7891–7900. https://doi.org/10.1021/bi3006708
doi: 10.1021/bi3006708