Abstract
This study explores the chemotactic potential of Bacillus subtilis MB378 against industrial dyes. Initial screening with swim plate assay showed significant movement of Bacillus subtilis MB378 towards test compounds. According to quantitative capillary assay, B. subtilis MB378 exhibited high chemotaxis potential towards Acid Orange 52 (CI: 9.52), followed by Direct Red 28 (CI: 8.39) and Basic Green 4 (CI: 5.21) in glucose-supplemented medium. Sequencing and gene annotation results evidently showed presence of chemotaxis genes and flagellar motor proteins in Bacillus subtilis draft genome. Methyl-accepting proteins (involved in chemotaxis regulation) belonged to pfam00672, pfam00072, and pfam00015 protein families. Annotated chemotaxis machinery of MB378 comprised 8 Che genes, 5 chemoreceptor genes, associated flagellar proteins, and rotary motors. Chemotaxis genes of B. subtilis MB378 were compared with genes of closely related Bacillus strains (168, WK1, and HTA426), depicting highly conserved regions showing evolutionary relation between them. Considering results of present study, it can be speculated that test compounds triggered chemotactic genes, which made these compounds bioavailable to the bacterium. Hence, the bacterium recognized and approached these compounds and facilitated biodegradation and detoxification of these compounds.
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Ahmad F, Zhu D, Sun J (2020) Bacterial chemotaxis: a way forward to aromatic compounds biodegradation. Environ Sci Eur 32:52. https://doi.org/10.1186/s12302-020-00329-2
Alexander G, Zhulin IB (2001) More than one way to sense chemicals. J Bacteriol 183:4681–4686
Alexander RP, Zhulin IB (2007) Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci U S A 104:2885–2890
Alexander G, Greer SE, Zhulin IB (2000) Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 18:6042–6048
Arora PK, Bae H (2014) Biotransformation and chemotaxis of 4-chloro-2-nitrophenol by Pseudomonas sp. JHN Microb Cell Fact 13:110–116
Arora PK, Jeong M-J, Bae H (2015) Chemotaxis away from 4-chloro-2-nitrophenol, 4-nitrophenol, and 2,6-dichloro-4-nitrophenol by Bacillus subtilis PA-2. J Chemother 2015:4. https://doi.org/10.1155/2015/296231
Asses N, Ayed L, Hkiri N, Hamdi M (2018) Congo Red decolorization and detoxification by Aspergillus niger: removal mechanisms and dye degradation pathway. BioMed Res Intl 2018:1–9. https://doi.org/10.1155/2018/3049686
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Berleman JE, Bauer CE (2005a) A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Mol Microbiol 55:1390–1402
Berleman JE, Bauer CE (2005b) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol 56:1457–1466
Bhattacharya S, Das A, Mangai G, Vignesh K, Sangeetha J (2011) Mycoremediation of Congo Red dye by filamentous fungi. Braz J Microbiol 42:1526–1536
Boesch KC, Silversmith RE, Bourret RB (2000) Isolation and characterization of nonchemotactic CheZ mutants of Escherichia coli. J Bacteriol 182:3544–3552
Cedar H (1988) DNA methylation and gene activity. Cell 53:3–4
Celani A, Vergassola M (2010) Bacterial strategies for chemotaxis response. Proc Natl Acad Sci USAm 107(4):1391–1396. https://doi.org/10.1073/pnas.0909673107
Derr P, Boder E, Goulian M (2006) Changing the specificity of a bacterial chemoreceptor. J Mol Biol 355:923–932
Egbert MD (2013) Bacterial chemotaxis: introverted or extroverted? A comparison of the advantages and disadvantages of basic forms of metabolism-based and metabolism independent behavior using a computational model. PLoS One 8(5):e63617. https://doi.org/10.1371/journal.pone.0063617
Egbert MD, Barandiaran XE, Di-Paolo EA (2010) A minimal model of metabolism-based chemotaxis. PLoS Comput Biol 6(12):e1001004. https://doi.org/10.1371/journal.pcbi.1001004
Faldu PR, Kothari VV, Kothari CR, Rawal CM, Domadia KK, Patel PA, Bhimani HD, Raval VH, Parmar NR, Nathani NM, Koringa PG, Joshi CG, Kothari RK (2014) Draft genome sequence of textile azo dye-decolorizing and -degrading Pseudomonas aeruginosa strain PFK10, isolated from the common effluent treatment plant of the Ankleshwar industrial area of Gujarat, India. Genome Announc 2(1):e00019–e00014. https://doi.org/10.1128/genomeA.00019-14
Falke JJ, Hazelbauer GL (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26:257–265
Fuentes I, Ccorahua R, Tinoco O, León O, Ramírez P (2019) Draft genome sequences of two textile azo dye-degrading Shewanella sp. strains isolated from a textile effluent in Peru. Microbiol Resour Announc 8:e00836–e00819. https://doi.org/10.1128/MRA.00836-19
Gordillo F, Chavez FP, Jerez CA (2007) Motility and chemotaxis of Pseudomonas sp. B4 towards polychlorobiphenyls and chlorobenzoates. FEMS Microbiol Ecol 60:322–328
Hess JF, Oosawa K, Kaplan N, Simon MI (1988) Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53:79–87
Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation throughnmodulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422–14427
Hong Y-H, Ye C-C, Zhou Q-Z, Wu X-Y, Yuan J-P, Peng J, Deng H, Wang J-H (2017) Genome sequencing reveals the potential of Achromobacter sp. HZ01 for bioremediation. Front Microbiol 8:1507
Junjie Z, Yufeng X, Hong L, Shujun W, Ningyi Z (2008) Metabolism-independent chemotaxis of Pseudomonas sp. strain WBC-3 toward aromatic compounds. J Environ Sci 20:1238–1242
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Kumar S, Vikram S, Raghava GPS (2013) Genome Annotation of Burkholderia sp. SJ98 with special focus on chemotaxis genes. PLoS One 8(8):e70624. https://doi.org/10.1371/journal.pone.0070624
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJY, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinform. 23:2947–2948
Leungsakul T, Keenan BG, Smets BF, Wood TK (2005) TNT and nitroaromatic compounds are chemoattractants for Burkholderia cepacia R34 and Burkholderia sp. strain DNT. Appl Microbiol Biotechnol 69:321–325
Lopes JG, Sourjik V (2018) Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut. ISME J 12:2736–2747. https://doi.org/10.1038/s41396-018-0227-5
Lux R, Shi W (2004) Chemotaxis-guided movements in bacteria. Crit Rev Oral Biol Med 15(4):207–220
McNally DF, Matsumura P (1991) Bacterial chemotaxis signaling complexes: formation of a CheA/CheW complex enhances autophosphorylation and affinity for CheY. Proc Natl Acad Sci U S A 88:6269–6273
Mukherjee T, Kumar D, Burriss N, Xie Z, Alexandre G (2016) Azospirillum brasilense chemotaxis depends on two signaling pathways regulating distinct motility parameters. J Bacteriol 198:1764–1772
Oosawa K, Hess JF, Simon MI (1988) Mutants defective in bacterial chemotaxis show modified protein phosphorylation. Cell 53:89–96
Ortega-Calvo JJ, Marchenko AI, Vorobyov AV, Borovick RV (2003) Chemotaxis in polycyclic aromatic hydrocarbon-degrading bacteria isolated from coal-tar- and oil-polluted rhizospheres. FEMS Microbiol Ecol 44:373–381
Pailan S, Saha P (2015) Chemotaxis and degradation of organophosphate compound by a novel moderately thermo-halo tolerant Pseudomonas sp. strain BUR11: evidence for possible existence of two pathways for degradation. PeerJ 3:e1378. https://doi.org/10.7717/peerj.1378
Pandey G, Jain RK (2002) Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol 68(12):5789–5795
Pandey G, Chauhan A, Samanta SK, Jain RK (2002) Chemotaxis of a Ralstonia sp. SJ98 towards co-metabolizable nitroaromatic compounds. Biochem Biophys Res Commun 299:404–409
Pandey J, Sharma NK, Khan F, Ghosh A, Oakeshott JG, Jain RK, Pandey G (2012) Chemotaxis of Burkholderia sp. strain SJ98 towards chloronitroaromatic compounds that it can metabolise. BMC Microbiol 12:19–21
Patnaik PR (2012) Noise in bacterial chemotaxis: sources, analysis and control. BioSci. 629(12):1030–1038. https://doi.org/10.1525/bio.2012.62.12.5
Pereira M, Parente JA, Bataus LAM, das Dores de Paula Cardoso D, Soares RBA, de Almeida Soares CA (2004) Chemotaxis and flagellar genes of Chromobacterium violaceum. Genet Mol Res 3(1):92–101
Porter SL, Wadhams GH, Armitage JP (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9:153–165
Rao CV, Glekas GD, Ordal GW (2008) The three adaptation systems of Bacillus subtilis chemotaxis. Trends Microbiol 16(10):480–487. https://doi.org/10.1016/j.tim.2008.07.003
Sanders DA, Gillece-Castro BL, Stock AM, Burlingame AL, Koshland DE Jr (1989) Identification of the site of phosphorylation of the chemotaxis response regulator protein. CheY J Biol Chem 264:21770–21778
Silversmith RE, Levin MD, Schilling E, Bourret RB (2008) Kinetic characterization of catalysis by the chemotaxis phosphatase CheZ Modulation of activity by the phosphorylated CheY substrate. J Biol Chem 283:756–765
Singh R, Olson MS (2008) Application of bacterial swimming and chemotaxis for enhanced bioremediation. In: Shah V (ed) Emerging Environmental Technologies. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8786-8_7
Stolz B, Berg HC (1991) Evidence for interactions between MotA and MotB, torque-generating elements of the flagellar motor of Escherichia coli. J Bacteriol 173:7033–7037
Szurmant H, Ordal GW (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68(2):301–319
Tahir U, Yasmin A (2019) Role of bacterial extracellular polymeric substances (EPS) in uptake and accumulation of co-contaminants. Int J Environ Sci Technol 16:8081–8092. https://doi.org/10.1007/s13762-019-02360-0
Tahir U, Yasmin A (2021) Decolorization and discovery of metabolic pathway for the degradation of Mordant Black 11 dye by Klebsiella sp. MB398. Braz J Microbiol 52:761–771. https://doi.org/10.1007/s42770-021-00470-x
Tahir U, Nawaz S, Khan UH, Yasmin A (2021) Assessment of biodecolorization potentials of biofilm forming bacteria from two different genera for Mordant Black 11 dye. Bioremed J. https://doi.org/10.1080/10889868.2021.1911920
Tola YH, Fujitani Y, Tani A (2019) Bacteria with natural chemotaxis towards methanol revealed by chemotaxis fishing technique. Biosci Biotechnol Biochem 83(11):2163–2171. https://doi.org/10.1080/09168451.2019.1637715
Vladimirov N, Sourjik V (2009) Chemotaxis: how bacteria use memory. Biol Chem 390(11):1097–1104. https://doi.org/10.1515/BC.2009.130
Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1025–1037
Wang H, Matsumura P (1996) Characterization of the CheAS/CheZ complex: a specific interaction resulting in enhanced dephosphorylating activity on CheY phosphate. Mol Microbiol 19:695–703
Wang X, Atencia J, Ford RM (2015) Quantitative analysis of chemotaxis towards toluene by Pseudomonas putida in a convection-free microfluidic device. Biotechnol Bioeng 112(5):896–904
Wang Y-H, Huang Z, Liu S-J (2019a) Chemotaxis towards aromatic compounds: insights from Comamonas testosteroni. Int J Mol Sci 20(11):2701. https://doi.org/10.3390/ijms20112701
Wang Y-H, Huang Z, Liu S-J (2019b) Chemotaxis towards aromatic compounds: insights from Comamonas testosterone. Int J Mol Sci 20:2701. https://doi.org/10.3390/ijms20112701
Whitchurch CB, Leech AJ, Young MD, Kennedy D, Sargent JL, Bertrand JJ, Semmler AB, Mellick AS, Martin PR, Alm RA, Hobbs M, Beatson SA, Huang B, Nguyen L, Commolli JC, Engel JN, Darzins A, Mattick JS (2004) Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol Microbiol 52:873–893
Acknowledgements
Whole genome sequencing was done at Ramaciotti Centre for Genomics, University of New South Wales, Sydney, Australia.
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Uruj Tahir: Conceptualization and designed experiments, methodology, data curation, formal analysis, investigation, visualization, and writing (original draft, review and editing). Azra Yasmin: Supervision and resources. Fozia Aslam: Data curation. Umair Hassan Khan and Shiza Nawaz: Writing (draft, review and editing).
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Tahir, ., Aslam, F., Nawaz, S. et al. Annotation of chemotaxis gene clusters and proteins involved in chemotaxis of Bacillus subtilis strain MB378 capable of biodecolorizing different dyes. Environ Sci Pollut Res 29, 3510–3520 (2022). https://doi.org/10.1007/s11356-021-15634-3
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DOI: https://doi.org/10.1007/s11356-021-15634-3


