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Transcriptome analysis provides new insights into the tolerance and reduction of Lysinibacillus fusiformis 15–4 to hexavalent chromium

  • Genomics, Transcriptomics, Proteomics
  • Published:
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Abstract  

Microbial bioremediation of Cr(VI)-contaminated environments has drawn extensive concern. However, the molecular processes underlying the microbial Cr(VI) tolerance and reduction remain unclear. We isolated a Cr(VI)-reducing Lysinibacillus fusiformis strain 15–4 from soil on the Qinghai-Tibet Plateau. When grown in 1 mM and 2 mM Cr(VI)-containing medium, strain 15–4 could reduce 100% and 93.7% of Cr(VI) to Cr(III) after 36 h and 60 h of incubation, respectively. To know the molecular processes in response to Cr(VI), transcriptome sequencing was carried out using RNA-Seq technology. The results annotated a total of 3913 expressed genes in the strain. One thousand ninety-eight genes (28.1%) were significantly (fold change ≥ 2, false discovery rate ≤ 0.05) expressed in response to Cr(VI), of which 605 (55.1%) were upregulated and 493 (44.9%) were downregulated. The enrichment analysis showed that a total of 630 differentially expressed genes (DEGs) were enriched to 122 KEGG pathways, of which 8 pathways were significantly (p < 0.05) enriched in Cr(VI)-treated sample, including ATP-binding cassette (ABC) transporters (97 DEGs), ribosome (40), sulfur metabolism (16), aminoacyl-tRNA biosynthesis (19), porphyrin metabolism (20), quorum sensing (44), oxidative phosphorylation (17), and histidine metabolism (10), suggesting that these pathways play key roles to cope with Cr(VI) in the strain. The highly upregulated DEGs consisted of 29 oxidoreductase, 18 dehydrogenase, 14 cell redox homeostasis and stress response protein, and 10 DNA damage and repair protein genes. However, seven Na+:H+ antiporter complex-coding DEGs and most of transcriptional regulator-coding DEGs were significantly downregulated in the Cr-treated sample. Many of FMN/NAD(P)H-dependent reductase-encoding genes were greatly induced by Cr, suggesting the involvement of these genes in Cr(VI) reduction in strain 15–4. Sulfur and iron ions as well as the thiol-disulfide exchange reactions might play synergistic roles in Cr reduction.

Key points

• Lysinibacillus fusiformis 15–4 was able to tolerate and reduce Cr(VI) to Cr(III).

• Transcriptome analysis revealed that 1098 DEGs and 8 key KEGG pathways significantly responded to Cr(VI).

• Sulfur metabolism, protein biosynthesis, and porphyrin metabolism were the key pathways associated with the survival of strain 15–4 in response to Cr(VI).

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Data and material for this article are available upon request.

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References

  • Ackerley D, Gonzalez C, Keyhan M, Blake R, Matin A (2004) Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6:851–860

    Article  CAS  PubMed  Google Scholar 

  • Aguilar-Barajas E, Paluscio E, Cervantes C, Rensing C (2008) Expression of chromate resistance genes from Shewanella sp. strain ANA-3 in Escherichia coli. FEMS Microbiol Lett 285:97–100

    CAS  PubMed  Google Scholar 

  • Ahemad M (2014) Bacterial mechanisms for Cr(VI) resistance and reduction: an overview and recent advances. Folia Microbiol 59:321–332

    Article  CAS  Google Scholar 

  • Ahmed I, Yokota A, Yamazoe A, Fujiwara T (2007) Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int J Syst Evol Microbiol 57:1117–1125

    Article  CAS  PubMed  Google Scholar 

  • Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    Article  CAS  PubMed  Google Scholar 

  • Bafana A, Chakrabarti T, Krishnamurthi K (2015) Mercuric reductase activity of multiple heavy metal-resistant Lysinibacillus sphaericus G1. J Basic Microbiol 55:285–292

    Article  CAS  PubMed  Google Scholar 

  • Bai YN, Lu YZ, Shen N, Lau TC, Zeng RJ (2018) Investigation of Cr(VI) reduction potential and mechanism by Caldicellulosiruptor saccharolyticus under glucose fermentation condition. J Hazard Mater 344:585–592

    Article  CAS  PubMed  Google Scholar 

  • Belchik SM, Kennedy DW, Dohnalkova AC, Wang Y, Sevinc PC, Wu H, Lin Y, Lu HP, Fredrickson JK, Shi L (2011) Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77:4035–4041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonilla JO, Callegari EA, Delfini CD, Estevez MC, Villegas LB (2016) Simultaneous chromate and sulfate removal by Streptomyces sp. MC1 changes in intracellular protein profile induced by Cr(VI). J Basic Microbiol 56:1212–1221

    Article  CAS  PubMed  Google Scholar 

  • Bowman B (1983) Vanadate uptake in Neurospora crassa occurs via phosphate transport system II. J Bacteriol 153:286–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Branco R, Chung AP, Johnston T, Gurel V, Morais P, Zhitkovich A (2008) The chromate-inducible chrBACF operon from the transposable element TnOtChr confers resistance to chromium(VI) and superoxide. J Bacteriol 190:6996–7003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brent R, Ptashne M (1981) Mechanism of action of the lexA gene product. Proc Natl Acad Sci USA 78:4204–4208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown SD, Thompson MR, Verberkmoes NC, Chourey K, Shah M, Zhou J, Hettich RL, Thompson DK (2006) Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol Cell Proteomics 5:1054–1071

    Article  CAS  PubMed  Google Scholar 

  • Brunker P, Rother D, Sedlmeier R, Klein J, Mattes R, Altenbuchner J (1996) Regulation of the operon responsible for broad-spectrum mercury resistance in Streptomyces lividans 1326. Mol Gen Genet 251:307–315

    CAS  PubMed  Google Scholar 

  • Burguiere P, Auger S, Hullo MF, Danchin A, Martin-Verstraete I (2004) Three different systems participate in L-cystine uptake in Bacillus subtilis. J Bacteriol 186:4875–4884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cervantes C, Campos-Garcia J, Devars S, Gutierrez-Corona F, Loza-Tavera H, Torres-Guzman JC, Moreno-Sanchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  PubMed  Google Scholar 

  • Chai L, Ding C, Li J, Yang Z, Shi Y (2019) Multi-omics response of Pannonibacter phragmitetus BB to hexavalent chromium. Environ Pollut 249:63–73

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Khaleel SS, Huang H, Wu CH (2014) Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol Med 9:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59:8

    Article  CAS  Google Scholar 

  • Gang H, Xiao C, Xiao Y, Yan W, Bai R, Ding R, Yang Z, Zhao F (2019) Proteomic analysis of the reduction and resistance mechanisms of Shewanella oneidensis MR-1 under long-term hexavalent chromium stress. Environ Int 127:94–102

    Article  CAS  PubMed  Google Scholar 

  • Garti-Levi S, Hazan R, Kain J, Fujita M, Ben-Yehuda S (2008) The FtsEX ABC transporter directs cellular differentiation in Bacillus subtilis. Mol Microbiol 69:1018–1028

    Article  CAS  PubMed  Google Scholar 

  • Graumann P, Marahiel MA (1994) The major cold shock protein of Bacillus subtilis CspB binds with high affinity to the ATTGG- and CCAAT sequences in single stranded oligonucleotides. FEBS Lett 338:157–160

    Article  CAS  PubMed  Google Scholar 

  • Gul N, Poolman B (2013) Functional reconstitution and osmoregulatory properties of the ProU ABC transporter from Escherichia coli. Mol Membr Biol 30:138–148

    Article  PubMed  Google Scholar 

  • He M, Li X, Liu H, Millerc SJ, Wang G, Rensing C (2011) Characterization and genomic analysis of a highly chromate resistant and reducing bacterial strain Lysinibacillus fusiformis ZC1. J Hazard Mater 185:682–688

    Article  CAS  PubMed  Google Scholar 

  • He Y, Dong L, Zhou S, Jia Y, Gu R, Bai Q, Gao J, Li Y, Xiao H (2018) Chromium resistance characteristics of Cr(VI) resistance genes ChrA and ChrB in Serratia sp. S2. Ecotox Envrion Saf 157:417–423

    Article  CAS  Google Scholar 

  • Henne KL, Turse JE, Nicora CD, Lipton MS, Tollaksen SL, Lindberg C, Babnigg G, Giometti CS, Nakatsu CH, Nakatsu DK, Konopka AE (2009) Global proteomic analysis of the chromate response in Arthrobacter sp strain FB24. J Proteome Res 8:1704–1716

    Article  CAS  PubMed  Google Scholar 

  • Hobbs EC, Yin X, Paul BJ, Astarita JL, Storz G (2012) Conserved small protein associates with the multidrug efflux pump AcrB and differentially affects antibiotic resistance. Proc Natl Acad Sci USA 109:16696–16701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu P, Brodie EL, Suzuki Y, McAdams HH, Andersen GL (2005) Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Bacteriol 187:8437–8449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez-Mejia R, Campos-Garcia J, Cervantes C (2006) Membrane topology of the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol Lett 262:178–184

    Article  CAS  PubMed  Google Scholar 

  • Kajiyama Y, Otagiri M, Sekiguchi J, Kosono S, Kudo T (2007) Complex formation by the mrpABCDEFG gene products which constitute a principal Na+/H+ antiporter in Bacillus subtilis. J Bacteriol 189:7511–7514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klopfenstein DV, Zhang L, Pedersen BS, Ramírez F, Warwick Vesztrocy A, Naldi A, Mungall CJ, Yunes JM, Botvinnik O, Weigel M, Dampier W, Dessimoz C, Flick P, Tang H (2018) GOATOOLS: a Python library for Gene Ontology analyses. Sci Rep 18:10872

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MJ, Kim HJ, Lee JY, Kwon AS, Jun SY, Kang SH, Kim P (2013) Effect of gene amplifications in porphyrin pathway on heme biosynthesis in a recombinant Escherichia coli. J Microbiol Biotechnol 23:668–673

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li NJ, Zeng GM, Huang DL, Huang C, Lai C, Wei Z, Xu P, Zhang C, Cheng M, Yan M (2015) Response of extracellular carboxylic and thiol ligands (oxalate thiol compounds) to Pb2+ stress in Phanerochaete chrysosporium. Environ Sci Pollut Res 22:12655–12663

    Article  CAS  Google Scholar 

  • Li SW, Huang YX, Liu MY (2020) Transcriptome profiling reveals the molecular processes for survival of Lysinibacillus fusiformis strain 15–4 in petroleum environments. Ecotoxicol Environ Saf 192:110250

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-△△Ct method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lozano LC, Dussán J (2013) Metal tolerance and larvicidal activity of Lysinibacillus sphaericus. World J Microbiol Biotechnol 29:1383–1389

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka H, Hirooka K, Fujita Y (2007) Organization and function of the YsiA regulon of Bacillus subtilis involved in fatty acid degradation. J Biol Chem 282:5180–5194

    Article  CAS  PubMed  Google Scholar 

  • Miranda AT, Gonzalez MV, Gonzalez G, Vargas E, Campos-Garcia J, Cervantes C (2005) Involvement of DNA helicases in chromate resistance by Pseudomonas aeruginosa PAO1. Mutat Res 578:202–209

    Article  CAS  PubMed  Google Scholar 

  • Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, Van Der Lelie D, Mergeay M (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 189:7417–7425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monsieurs P, Moors H, Van Houdt R, Janssen PJ, Janssen A, Coninx I, Mergeay M, Leys N (2011) Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network. Biometals 24:1133–1151

    Article  CAS  PubMed  Google Scholar 

  • Morohoshi F, Hayashi K, Munakata N (1990) Bacillus subtilis ada operon encodes two DNA alkyltransferases. Nucleic Acids Res 18:5473–5480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  PubMed  Google Scholar 

  • Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188:3664–3673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park SG, Cha MK, Jeong W, Kim IH (2000) Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J Biol Chem 275:5723–5732

    Article  CAS  PubMed  Google Scholar 

  • Prithviraj D, Deboleena K, Neelu N, Noor N (2014) Biosorption of nickel by Lysinibacillus sp BA2 native to bauxite mine. Ecotoxicol Environ Saf 107:260–268

    Article  CAS  PubMed  Google Scholar 

  • Rahman A, Nahar N, Nawani NN, Jass J, Ghosh S, Olsson B, Mandal A (2015) Genomics comparative genome analysis of Lysinibacillus B1-CDA a bacterium that accumulates arsenics. Genomics 106:384–392

    Article  CAS  PubMed  Google Scholar 

  • Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368–375

    Article  CAS  PubMed  Google Scholar 

  • Ren S, Li Q, Xie L, Xie J (2017) Molecular mechanisms underlying the function diversity of ArsR family metalloregulator. Crit Rev Eukar Gene 27:19–35

    Article  Google Scholar 

  • Robins KJ, Hooks DO, Rehm BH, Ackerley DF (2013) Escherichia coli NemA is an efficient chromate reductase that can be biologically immobilized to provide a cell free system for remediation of hexavalent chromium. PLoS ONE 8:e59200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) dgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Scott AI, Roessner CA (2002) Biosynthesis of cobalamin (vitamin B12). Biochem Society Trans 30:613–620

    Article  CAS  Google Scholar 

  • Shaw DR, Dussan J (2018) Transcriptional analysis and molecular dynamics simulations reveal the mechanism of toxic metals removal and efflux pumps in Lysinibacillus sphaericus OT4b31. Inter Biodeter Biodegr 127:46–61

    Article  CAS  Google Scholar 

  • Suzuki T, Miyata N, Horitsu H, Kawai K, Takamizawa K, Tai Y, Okazaki M (1992) NAD(P)H-dependent chromium (VI) reductase of Pseudomonas ambigua G-1: a Cr(V) intermediate is formed during the reduction of Cr(VI) to Cr (III). J Bacteriol 174:5340–5345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson DK, Chourey K, Wickham GS, Thieman SB, Verberkmoes NC, Zhang B, McCarthy AT, Rudisill MA, Shah M, Hettich RL (2010) Proteomics reveals a core molecular response of Pseudomonas putida F1 to acute chromate challenge. BMC Genomics 11:311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-Seq. Nat Biotechnol 31:46–53

    Article  CAS  PubMed  Google Scholar 

  • Trotter EW, Grant CM (2002) Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol Microbiol 46:869–878

    Article  CAS  PubMed  Google Scholar 

  • Urone PF (1955) Stability of colorimetric reagent for chromium S-diphenylcarbazide in various solvents. Anal Chem 27:1354–1355

    Article  CAS  Google Scholar 

  • Viamajala S, Peyton BM, Apel WA, Petersen JN (2002) Chromate/nitrite interactions in Shewanella oneidensis MR-1: evidence for multiple hexavalent chromium [Cr(VI)] reduction mechanisms dependent on physiological growth conditions. Biotechnol Bioeng 78:770–778

    Article  CAS  PubMed  Google Scholar 

  • Viti C, Decorosi F, Tatti E, Giovannetti L (2007) Characterization of chromate-resistant and -reducing bacteria by traditional means and by a high-throughput phenomic technique for bioremediation purposes. Biotechnol Prog 23:553–559

    Article  CAS  PubMed  Google Scholar 

  • Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol 38:633–659

    Article  CAS  Google Scholar 

  • Wu R, Skaar EP, Zhang R, Joachimiak G, Gornicki P, Schneewind O, Joachimiak A (2005) Staphylococcus aureus IsdG and IsdI heme-degrading enzymes with structural similarity to monooxygenases. J Biol Chem 280:2840–2846

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Liu L, Zeng GM, Huang DL, Lai C, Zhao MH, Huang C, Li N, Wei Z, Wu H, Zhang C, Lai M, He Y (2014) Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 98:6409–6418

    Article  CAS  PubMed  Google Scholar 

  • Yu G, Wang LG, Han Y (2012) He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Q, Hu Y, Yang Y, Hu L, Zhong H, He Z (2019) Cell envelop is the key site for Cr(VI) reduction by Oceanobacillus oncorhynchi W4 a newly isolated Cr(VI) reducing bacterium. J Hazard Mater 368:149–155

    Article  CAS  PubMed  Google Scholar 

  • Zenno S, Kobori T, Tanokura M, Saigo K (1998) Purification and characterization of NfrA1 a Bacillus subtilis nitro/flavin reductase capable of interacting with the bacterial luciferase. Biosci Biotechnol Biochem 62:1978–1987

    Article  CAS  PubMed  Google Scholar 

  • Zhang JK, Wang ZH, Ye Y (2016) Heavy metal resistances and chromium removal of a novel Cr(VI)-reducing pseudomonad strain isolated from circulating cooling water of iron and steel plant. Appl Biochem Biotechnol 180:1328–1344

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wu W, Virgo N, Zou L, Liu P, Li X (2014) Global transcriptome analysis of hexavalent chromium stress responses in Staphylococcus aureus LZ-01. Ecotoxicology 23:1534–1545

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Li Y, Zhang X, Liu P, Ren J, Wu G, Zheng Y, Chen Y, Li X (2015) A Bacillus subtilis strain can reduce hexavalent chromium to trivalent and an nfrA gene is involved. Inter Biodeter Biodegr 97:90–96

    Article  CAS  Google Scholar 

  • Zhu Y, Yan J, Xia L, Zhang X, Luo L (2019) Mechanisms of Cr(VI) reduction by Bacillus sp CRB-1 a novel Cr(VI)-reducing bacterium isolated from tannery activated sludge. Ecotox Environ Saf 186:109792

    Article  CAS  Google Scholar 

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Funding

This work was funded by the National Natural Science Foundation of China (No. 31760110).

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Authors and Affiliations

  1. School of Environmental and Municipal Engineering, Lanzhou Jiaotong University, Lanzhou, People’s Republic of China

    Shi-Weng Li

  2. School of Chemical and Biological Engineering, Lanzhou Jiaotong University, Lanzhou, 730070, People’s Republic of China

    Shi-Weng Li, Ya Wen & Yan Leng

  3. Key Laboratory of Extreme Environmental Microbial Resources and Engineering in Gansu Province, Lanzhou, 730000, People’s Republic of China

    Shi-Weng Li

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  1. Shi-Weng Li
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SL conceived and designed research and wrote the manuscript. YW and YL conducted experiments and analyzed data. All authors read and approved the manuscript.

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Correspondence to Shi-Weng Li.

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Li, SW., Wen, Y. & Leng, Y. Transcriptome analysis provides new insights into the tolerance and reduction of Lysinibacillus fusiformis 15–4 to hexavalent chromium. Appl Microbiol Biotechnol 105, 7841–7855 (2021). https://doi.org/10.1007/s00253-021-11586-3

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