Enhanced Bioremediation Potential of Shewanella decolorationis RNA Polymerase Mutants and Evidence for Novel Azo Dye Biodegradation Pathways
Open accessAbstract
Bioremediation has been considered as a promising method for recovering chemical polluted environments. Here Shewanella decolorationis strain Ni1-3 showed versatile abilities in bioremediation. To improve the bioremediation activity, RNA polymerase (RNAP) mutations of strain Ni1-3 were screened. Eleven mutants were obtained, of which mutant #40 showed enhanced Amaranth (AMR) degradation capacity, while mutant #21 showed defected capacity in AMR degradation but greatly enhanced capacity in cathodic metal leaching which is three to four times faster than that of the wild-type (WT) strain Ni1-3, suggesting that different pathways were involved in these two processes. Transcriptional profiling and gene co-expression networks between the mutants (i.e., #40 and #22) and the WT strain disclosed that the non-CymA-Mtr but cytochrome b- and flavin-oxidoreductase-dominated azo dye degradation pathways existed in S. decolorationis, which involved key proteins TorC, TorA, YceJ, YceI, Sye4, etc. Furthermore, the involvement of TorA was verified by trimethylamine N-oxide reduction and molybdenum enzyme inhibitory experiments. This study clearly demonstrates that RNAP mutations are effective to screen active microbial candidates in bioremediation. Meanwhile, by clarifying the novel gene co-expression network of extracellular electron transfer pathways, this study provides new insights in azo dye degradation and broadens the application of Shewanella spp. in bioremediation as well.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Shewanella spp. can break down solid oxidized metals in used LIBs, such as Ni(IV), Co(IV), and Mn(IV).
“It has been seen that Shewanella spp.can break down solid oxidized metals in used LIBs, such as Ni (IV), Co (IV), and Mn (IV).”
From Harnessing bacterial consortia for effective bioremediation: targeted removal of heavy metals, hydrocarbons, and persistent pollutants (2025) · cites this paper as [49]
The Results and Discussion report that S. decolorationis and its mutants bioleached Ni, Co, and Mn from spent lithium-ion battery cathode material. But the Introduction says reduction of the specifically listed Ni(IV), Co(IV), and Mn(IV) in those batteries *might* occur; the reported leaching does not establish that those oxidation states were reduced. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCai et al. demonstrate that RNAP mutations effectively screen bioremediation candidates, clarify gene co-expression networks, and expand the application of Shewanella spp. in azo dye removal.
“Furthermore, Cai et al. [49] demonstrate that RNAP mutations effectively screen bioremediation candidates, clarify gene co-expression networks, and expand the application of Shewanella spp. in azo dye removal.”
From Harnessing bacterial consortia for effective bioremediation: targeted removal of heavy metals, hydrocarbons, and persistent pollutants (2025) · cites this paper as [49]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Xin, Y., Guo, X., Chen, S., Wang, J., Wu, F., & Xin, B. (2016) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2016.01.001 · Cited by 306 · see citing works
Flagged first, then by citations
Research works printed but not linked: 57
- Ajaz M. Shakeel S. Rehman A. (2019). Microbial use for azo dye degradation-a strategy for dye bioremediation. Int. Microbiol. 23 149– 159. 10.1007/s10123-019-00103-2 31741129 · DOI
- Alifano P. Palumbo C. Pasanisi D. Talà A. (2015). Rifampicin-resistance, rpoB polymorphism and RNA polymerase genetic engineering. J. Biotechnol. 202 60– 77. 10.1016/j.jbiotec.2014.11.024 25481100 · DOI
- Bouillet S. Arabet D. Jourlin-Castelli C. Mejean V. Iobbi-Nivol C. (2018). Regulation of sigma factors by conserved partner switches controlled by divergent signalling systems. Env. Microbiol. Rep. 10 127– 139. 10.1111/1758-2229.12620 29393573 · DOI
- Boxall N. J. Cheng K. Y. Bruckard W. Kaksonen A. H. (2018). Application of indirect non-contact bioleaching for extracting metals from waste lithium-ion batteries. J. Hazard. Mater. 360 504– 511. 10.1016/j.jhazmat.2018.08.024 30144769 · DOI
- Breuer M. Rosso K. M. Blumberger J. Butt J. N. (2015). Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities. J. R. Soc. Interface 12 20141117. 10.1098/rsif.2014.1117 25411412 PMC4277109 · DOI
- Burns J. Ginn B. Bates D. Dublin S. Taylor J. Apkarian R. (2010). Outer membrane-associated serine protease involved in adhesion of Shewanella oneidensis to Fe(III) Oxides. Environ. Sci. Technol. 44 68– 73. 10.1021/es9018699 20039735 · DOI
- Cai P. J. Xiao X. He Y. R. Li W. W. Chu J. Wu C. (2011). Anaerobic biodecolorization mechanism of methyl orange by Shewanella oneidensis MR-1. Appl. Microbiol. Biotechnol. 93 1769– 1776. 10.1007/s00253-011-3508-8 21808969 · DOI
- Cai X. C. Xi H. Liang L. Liu J. D. Liu C. H. Xue Y. R. (2017). Rifampicin-resistance mutations in the rpoB Gene in Bacillus velezensis CC09 have pleiotropic effects. Front. Microbiol. 08: e178. 10.3389/fmicb.2017.00178 28243227 PMC5303731 · DOI
- Cai X. C. Zheng X. Zhang D. N. Iqbal W. Liu C. K. Yang B. (2019). Microbial characterization of heavy metal resistant bacterial strains isolated from an electroplating wastewater treatment plant. Ecotoxicol. Environ. Saf. 181 472– 480. 10.1016/j.ecoenv.2019.06.036 31228823 · DOI · Paper page
- Cao X. Qi Y. Xu C. Yang Y. Wang J. (2017). Transcriptome and metabolome responses of Shewanella oneidensis MR-1 to methyl orange under microaerophilic and aerobic conditions. Appl. Microbiol. Biotechnol. 101 3463– 3472. 10.1007/s00253-016-8087-2 28070664 · DOI
- Chen H. Luo Q. Yin J. Gao T. Gao H. (2015). Evidence for the requirement of CydX in function but not assembly of the cytochrome bd oxidase in Shewanella oneidensis. Biochim. Biophys. Acta 1850 318– 328. 25316290
- Chen X. J. Xu M. Y. Wei J. B. Sun G. P. (2010). Two different electron transfer pathways may involve in azoreduction in Shewanella decolorationis S12. Appl. Microbiol. Biotechnol. 86 743– 751. 10.1007/s00253-009-2376-y 20012540 · DOI
- Chung K. T. (2016). Azo dyes and human health: a review. J. Environ. Sci. Health C. Environ. Carcinog. Ecotoxicol. Rev. 34 233– 261. 10.1080/10590501.2016.1236602 27635691 · DOI
- Clarke T. White G. Edwards M. Gomez-Perez L. Richardson D. Butt J. (2016). Mechanisms of bacterial extracellular electron exchange. Adv. Microb. Physiol. 68 87– 138. 10.1016/bs.ampbs.2016.02.002 27134022 · DOI
- Dangi A. K. Sharma B. Hill R. T. Shukla P. (2019). Bioremediation through microbes: systems biology and metabolic engineering approach. Crit. Rev. Biotechnol. 39 79– 98. 10.1080/07388551.2018.1500997 30198342 · DOI
- Deblonde T. Cossu-Leguille C. Hartemann P. (2011). Emerging pollutants in wastewater: a review of the literature. Int. J. Hyg. Environ. Health 214 442– 448. 10.1016/j.ijheh.2011.08.002 21885335 · DOI
- Elegheert J. van Den Hemel D. Dix I. Stout J. van Beeumen J. Brigé A. (2010). Towards structural studies of the old yellow enzyme homologue SYE4 from Shewanella oneidensis and its complexes at atomic resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 85– 90. 10.1107/S1744309109050386 20057079 PMC2805545 · DOI
- Eslami M. Amoozegar M. A. Asad S. (2016). Isolation, cloning and characterization of an azoreductase from the halophilic bacterium Halomonas elongata. Int. J. Biol. Macromol. 85 111– 116. 10.1016/j.ijbiomac.2015.12.065 26724685 · DOI
- Fang Y. Liu J. Kong G. Liu X. Yang Y. Li E. (2019). Adaptive responses of Shewanella decolorationis to the toxic organic extracellular electron acceptor in anaerobic respiration. Appl. Environ. Microb. 85 e00550-19. 10.1128/AEM.00550-19 31175185 PMC6677847 · DOI
- Filomeno G. Feraco S. (2020). Economic, technical and environmental aspects of recycling lithium batteries: a literature review. Glob. J. Res. Eng. XX, 1– 8.
- Fries M. R. Zhou J. Chee-Sanford J. Tiedje J. M. (1994). Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl. Environ. Microb. 60 2802– 2810. 10.1128/aem.60.8.2802-2810.1994 8085824 PMC201726 · DOI
- Gupta H. Gupta B. (2016). Vehicular tire as potential adsorbent for the removal of polycyclic aromatic hydrocarbons. Polycycl. Aromat. Comp. 38 354– 368. 10.1080/10406638.2016.1217890 · DOI
- Heisler L. Feng G. Jin D. Gross C. Landick R. (1996). Amino acid substitutions in the two largest subunits of Escherichia coli RNA polymerase that suppress a defective Rho termination factor affect different parts of the transcription complex. J. Biol. Chem. 271 14572– 14583. 10.1074/jbc.271.24.14572 8662850 · DOI
- Hong Y. Xu M. Guo J. Xu Z. Chen X. Sun G. (2007). Respiration and growth of Shewanella decolorationis S12 with an azo compound as the sole electron acceptor. Appl. Environ. Microb. 73 64– 72. 10.1128/AEM.01415-06 17085710 PMC1797134 · DOI
- Imran M. Arshad M. Negm F. Khalid A. Shaharoona B. Hussain S. (2016). Yeast extract promotes decolorization of azo dyes by stimulating azoreductase activity in Shewanella sp. strain IFN4. Ecotoxicol. Environ. Saf. 124, 42– 49. 10.1016/j.ecoenv.2015.09.041 26454074 · DOI
- Ingham C. Furneaux P. A. (2001). Mutations in the β subunit of the Bacillus subtilis RNA polymerase that confer both rifampicin resistance and hypersensitivity to NusG. Microbiology 146(Pt. 12), 3041– 3049. 10.1099/00221287-146-12-3041 11101662 · DOI
- Jin D. J. Walter W. Gross C. (1988). Characterization of the termination phenotypes of rifampicin resistant rpoB mutants in Escherichia coli. J. Mol. Biol. 202 245– 253. 10.1016/0022-2836(88)90455-x 3050123 · DOI
- Khalid A. Arshad M. Crowley D. (2008). Decolorization of azo dyes by Shewanella sp. under saline conditions. Appl. Microbiol. Biotechnol. 79 1053– 1059. 10.1007/s00253-008-1498-y 18461315 · DOI
- Kim D. Langmead B. Salzberg S. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12 357– 360. 10.1038/nmeth.3317 25751142 PMC4655817 · DOI · Paper page
- Langfelder P. Horvath S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559. 10.1186/1471-2105-9-559 19114008 PMC2631488 · DOI · Paper page
- Larsson D. J. (2014). Pollution from drug manufacturing: review and perspectives. Philos. T. R. Soc. B. 369: 20130571. 10.1098/rstb.2013.0571 25405961 PMC4213584 · DOI
- Lemke R. A. S. Olson S. M. Morse K. Karlen S. D. Higbee A. Beebe E. T. (2020). A bacterial biosynthetic pathway for methylated furan fatty acids. J. Biol. Chem. 295 9786– 9801. 10.1074/jbc.RA120.013697 32434926 PMC7380195 · DOI
- Liu G. F. Zhou J. T. Chen C. Wang J. Jin R. Lv H. (2013a). Decolorization of azo dyes by Geobacter metallireducens. Appl. Microbiol. Biotechnol. 97 7935– 7942. 10.1007/s00253-012-4545-7 23132348 · DOI
- Liu G. F. Zhou J. T. Meng X. M. Fu S. Q. Wang J. Jin R. (2013b). Decolorization of azo dyes by marine Shewanella strains under saline conditions. Appl. Microbiol. Biotechnol. 97 4187– 4197. 10.1007/s00253-012-4216-8 22707057 · DOI
- Luan F. Burgos W. Xie L. Zhou Q. (2009). Bioreduction of nitrobenzene, natural organic matter, and hematite by Shewanella putrefaciens CN32. Environ. Sci. Technol. 44 184– 190. 10.1021/es901585z 19957913 · DOI
- Mani S. Chowdhary P. Bharagava R. (2019). “ Textile wastewater dyes: toxicity profile and treatment approaches,” in Emerging and Eco-Friendly Approaches for Waste Management eds Bharagava R. Chowdhary P. (Singapore: Springer Singapore), 219– 244. 10.1016/j.ecoenv.2019.110007 · DOI
- Mauro R. Tumolo M. Ancona V. Campanale C. De Paola D. Ardito C. (2019). “ Assessment of bioremediation efficiency for recovering hexavalent chromium contaminated groundwater: a batch laboratory scale study,” in Proceedings of the Remtech Europe 2019. Ferrara.
- Meng X. M. Liu G. F. Zhou J. T. Fu S. Q. Wang G. H. (2012). Azo dye decolorization by Shewanella aquimarina under saline conditions. Bioresource Technol. 14 95– 101. 10.1016/j.biortech.2012.03.003 22449986 · DOI
- Meyer T. E. Tsapin A. I. Vandenberghe I. de Smet L. Frishman D. Nealson K. H. (2004). Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8 57– 77. 10.1089/153623104773547499 15107237 · DOI
- Mintmier B. Nassif S. Stolz J. F. Basu P. (2020). Functional mononuclear molybdenum enzymes: challenges and triumphs in molecular cloning, expression, and isolation. J. Biol. Inorg. Chem. 25 547– 569. 10.1007/s00775-020-01787-y 32279136 · DOI
- Naaz S. Ghosh P. Vaidya A. Waindeskar V. Das S. Mudliar S. (2017). Comparison of coagulation, ozone and ferrate treatment processes for color, COD and toxicity removal from complex textile wastewater. Water Sci. Technol. 76: wst2017062. 10.2166/wst.2017.062 28876242 · DOI
- Patro R. Duggal G. Love M. Irizarry R. Kingsford C. (2017). Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14 417– 419. 10.1038/nmeth.4197 28263959 PMC5600148 · DOI · Paper page
- Popli S. Patel U. (2014). Destruction of azo dyes by anaerobic-aerobic sequential biological treatment: a review. Int. J. Environ. Sci. Technol. 12 405– 420.
- Puvaneswari N. Jayarama M. Gunasekaran P. (2006). Toxicity assessment and microbial degradation of azo dyes. Indian J. Exp. Biol. 44 618– 626. 16924831
- Robinson M. McCarthy D. Smyth G. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 139– 140. 10.1093/bioinformatics/btp616 19910308 PMC2796818 · DOI · Paper page
- Saratale R. Saratale G. Chang J. S. Govindwar S. (2011). Bacterial decolorization and degradation of azo dyes: a review. J. Taiwan Inst. Chem. Eng. 42 138– 157.
- Shannon P. Markiel A. Ozier O. Baliga N. Wang J. Ramage D. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 2498– 2504. 10.1101/gr.1239303 14597658 PMC403769 · DOI · Paper page
- Tang J. Kong D. Cui Q. Wang K. Zhang D. Gong Y. (2018). Prognostic genes of breast cancer identified by gene co-expression network analysis. Front. Oncol. 8: e374. 10.3389/fonc.2018.00374 30254986 PMC6141856 · DOI
- Venkata S. Prasad K. Rao N. Sarma P. (2005). Acid azo dye degradation by free and immobilized horseradish peroxidase (HRP) catalyzed process. Chemosphere 58 1097– 1105. 10.1016/j.chemosphere.2004.09.070 15664617 · DOI
- Vikrant K. Giri B. S. Raza N. Roy K. Kim K. H. Rai B. N. (2018). Recent advancements in bioremediation of dye: current status and challenges. Bioresource Technol. 253 355– 367. 10.1016/j.biortech.2018.01.029 29352640 · DOI
- Xiao X. Li T. T. Lu X. R. Feng X. L. Han X. Li W. W. (2018). A simple method for assaying anaerobic biodegradation of dyes. Bioresource Technol. 251 204– 209. 10.1016/j.biortech.2017.12.052 29277051 · DOI
- Xu X. Cheng Y. Zhang T. Ji F. Xu X. (2016). Treatment of pharmaceutical wastewater using interior micro-electrolysis/Fenton oxidation-coagulation and biological degradation. Chemosphere 152 23– 30. 10.1016/j.chemosphere.2016.02.100 26953729 · DOI
- Yang Y. G. Xiang Y. B. Sun G. P. Wu W. M. Xu M. Y. (2015). Electron acceptor-dependent respiratory and physiological stratifications in biofilms. Environ. Sci. Technol. 49 196– 202. 10.1021/es504546g 25495895 · DOI
- Yang Y. Han L. Yuan Y. Li J. Hei N. Liang H. (2014). Gene co-expression network analysis reveals common system-level properties of prognostic genes across cancer types. Nat. Commun. 5: 3231. 10.1038/ncomms4231 24488081 PMC3951205 · DOI · Paper page
- Zeng X. Li J. Singh N. (2014). Recycling of spent lithium-ion battery: a critical review. Crit. Rev. Env. Sci. Tec. 44 1129– 1165.
- Zhang H. Han K. Hu X. (2020). Enhanced bioreduction of 2,5-dichlorobenzene by an AHQ/RGO binary nanocomposite through a synergistic effect with outer membrane proteins of Shewanella oneidensis MR-1. Chem. Eng. J. 389: 124464. 10.1016/j.cej.2020.124464 · DOI
- Zhao G. Jiang L. He Y. Li J. Dong H. Wang X. (2011). Sulfonated graphene for persistent aromatic pollutant management. Adv. Mater. 23 3959– 3963. 10.1002/adma.201101007 21800380 · DOI
Cited by
Sorted by citations
Qattan, S. Y. A. (2025) · Environmental Sciences Europe · doi:10.1186/s12302-025-01103-y · Cited by 109 · see citing works
- Authors
- Cai, X., Zheng, X., Wang, Y., Tian, L., & Mao, Y.
- Affiliations
- Shenzhen University (CN)
- Corresponding author
- Mao, Yanping
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2022-03-22
- Volume
- 13
- Pages
- 843807-843807
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC8981235
- OpenAlex
- W4220755714
- Cited by
- 6
- References
- 1
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1
- FWCI
- 0.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (41907214, 51708358)
- Postdoctoral Research Foundation of China
- Topics
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Enzyme-mediated dye degradation
- Physical Sciences › Environmental Science › Pollution › Microbial bioremediation and biosurfactants
- Keywords
- azo dye biodegradation, extracellular electron transfer, gene co-expression network, TORA, bioremediation, gene expression profiling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review