The catE gene of Bacillus licheniformis M2-7 is essential for growth in benzopyrene, and its expression is regulated by the Csr system.
Benzopyrene
Csr system
Microbial growth
Posttranscriptional regulation
Journal
World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472
Informations de publication
Date de publication:
28 Apr 2023
28 Apr 2023
Historique:
received:
23
01
2023
accepted:
25
04
2023
medline:
1
5
2023
pubmed:
28
4
2023
entrez:
28
4
2023
Statut:
epublish
Résumé
Benzopyrene is a high-molecular-weight polycyclic aromatic hydrocarbon that is highly recalcitrant and induces carcinogenic effects. CsrA is a conserved regulatory protein that controls the translation and stability of its target transcripts, having negative or positive effects depending on the target mRNAs. It is known that Bacillus licheniformis M2-7 has the ability to grow and survive in certain concentrations of hydrocarbons such as benzopyrene, prompted in part by CsrA, as is present in gasoline. However, there are a few studies that reveal the genes involved in that process. To identify the genes involved in the Bacillus licheniformis M2-7 degradation pathway, the plasmid pCAT-sp containing a mutation in the catE gene was constructed and used to transform B. licheniformis M2-7 and generate a CAT1 strain. We determined the capacity of the mutant B. licheniformis (CAT1) to grow in the presence of glucose or benzopyrene as a carbon source. We observed that the CAT1 strain presented increased growth in the presence of glucose but a statistically considerable decrease in the presence of benzopyrene compared with the wild-type parental strain. Additionally, we demonstrated that the Csr system positively regulates its expression since it was observed that the expression of the gene in the mutant strain LYA12 (M2-7 csrA:: Sp, SpR) was considerably lower than that in the wild-type strain. We were thus able to propose a putative regulation model for catE gene in B. licheniformis M2-7 strain by CsrA regulator in the presence of benzopyrene.
Identifiants
pubmed: 37115273
doi: 10.1007/s11274-023-03630-3
pii: 10.1007/s11274-023-03630-3
doi:
Substances chimiques
Repressor Proteins
0
Transcription Factors
0
Benzo(a)pyrene
3417WMA06D
Benzopyrenes
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
177Subventions
Organisme : Consejo Nacional de Ciencia y Tecnología
ID : M.Sc. scholarships.
Organisme : SAGARPA-CONACYT
ID : 18-PFA-IIDTTT-000089-L000-DF
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Altegoer F, Rensing SA, Bange G (2016) Structural basis for the CsrA-dependent modulation of translation initiation by an ancient regulatory protein. Proc Natl Acad Sci 113:10168–10173. https://doi.org/10.1073/pnas.1602425113
doi: 10.1073/pnas.1602425113
pubmed: 27551070
pmcid: 5018767
Bhatt KK, Lily MK, Joshi G, Dangwal K (2018) Benzo(a)pyrene degradation pathway in Bacillus subtilis BMT4i (MTCC 9447). Turkish Journal of Biochemistry 43:693–701. https://doi.org/10.1515/tjb-2017-0334
doi: 10.1515/tjb-2017-0334
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
doi: 10.1016/0003-2697(76)90527-3
pubmed: 942051
Cébron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159. https://doi.org/10.1016/j.mimet.2008.01.009
doi: 10.1016/j.mimet.2008.01.009
pubmed: 18329116
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368. https://doi.org/10.1007/BF00129093
doi: 10.1007/BF00129093
Damm K, Bach S, Müller KM, Klug G, Burenina OY, Kubareva EA, Grünweller A, Hartmann RK (2015) Impact of RNA isolation protocols on RNA detection by Northern blotting. Methods Mol Biol 1296:29–38. https://doi.org/10.1007/978-1-4939-2547-6_4
doi: 10.1007/978-1-4939-2547-6_4
pubmed: 25791588
Diomandé SE, Nguyen-The C, Guinebretière MH, Broussolle V, Brillard J (2015) Role of fatty acids in Bacillus environmental adaptation. Front Microbiol 6:813–832. https://doi.org/10.3389/fmicb.2015.00813
doi: 10.3389/fmicb.2015.00813
pubmed: 26300876
pmcid: 4525379
Eskandari S, Hoodaji M, Tahmourespour A, Abdollahi A, Baghi TM, Eslamian S, Ostad-Ali-Askari K (2017) Bioremediation of polycyclic aromatic hydrocarbons by Bacillus licheniformis ATHE9 and Bacillus mojavensis ATHE13 as newly strains isolated from oil-contaminated soil. Journal of Geography, Environment and Earth Science International 11:1–11. https://doi.org/10.9734/JGEESI/2017/35447
doi: 10.9734/JGEESI/2017/35447
Fanali LZ, Franco-Belussi L, Bonini-Domingos CR, de Oliveira C (2018) Effects of benzo[a]pyrene on the blood and liver of Physalaemus cuvieri and Leptodactylus fuscus (Anura: Leptodactylidae). Environ Pollut 237:93–102. https://doi.org/10.1016/j.envpol.2018.02.030
doi: 10.1016/j.envpol.2018.02.030
pubmed: 29477119
Fellay R, Frey J, Krisch H (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of Gram-negative bacteria. Gene 52:147–154. https://doi.org/10.1016/0378-1119(87)90041-2
doi: 10.1016/0378-1119(87)90041-2
pubmed: 3038679
Guevara-Luna J, Alvarez-Fitz P, Ríos-Leal E, Acevedo-Quiroz M, Encarnación-Guevara S, Moreno-Godinez ME, Castellanos-Escamilla M, Toribio-Jiménez J, Romero-Ramírez Y (2018) Biotransformation of benzo[a]pyrene by the thermophilic bacterium Bacillus licheniformis M2-7. World J Microbiol Biotechnol 34:88. https://doi.org/10.1007/s11274-018-2469-9
doi: 10.1007/s11274-018-2469-9
pubmed: 29886516
Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243. https://doi.org/10.1271/bbb.67.225
doi: 10.1271/bbb.67.225
pubmed: 12728980
Hoffmann K, Wollherr A, Larsen M, Rachinger M, Liesegang H, Ehrenreich A, Meinhardt F (2010) Facilitation of direct conditional knockout of essential genes in Bacillus licheniformis DSM13 by comparative genetic analysis and manipulation of genetic competence. Appl Environ Microbiol 76:5046–5057. https://doi.org/10.1128/AEM.00660-10
doi: 10.1128/AEM.00660-10
pubmed: 20543043
pmcid: 2916460
Huisman GW, Siegele DA, Zambrano MA, Kolter R (1996) Morphological and physiological changes during stationary phase. In: Neidhardt F C, Curtiss III R, Ingraham J L, Lin E C C, Low K B, Magasanik B, Reznikoff W S, Riley M, Schaechter M, Umbarger H E, editors. Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. Washington DC, ASM Press, pp. 1672–1682. https://doi.org/10.1128/MMBR.65.1.119-130.2001
Ishida T, Kita A, Miki K, Nozaki M, Horiike K (2002) Structure and reaction mechanism of catechol 2,3-dioxygenase (metapyrocatechase). Int. Congr. Ser., Oxygen and life: Oxygenases, oxidase and lipid mediators 1233:213–220. https://doi.org/10.1016/S0531-5131(02)00149-8
Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia CE (2007) Complete and Integrated Pyrene Degradation Pathway in Mycobacterium vanbaalenii PYR-1 based on Systems Biology. J Bacteriol 189:464–472. https://doi.org/10.1128/JB.01310-06
doi: 10.1128/JB.01310-06
pubmed: 17085566
Kita A, Kita S, Fujisawa I, Inaka K, Ishida T, Horiike K, Nozaki M, Miki K (1999) An archetypical extradiol-cleaving catecholic dioxygenase: the crystal structure of catechol 2,3-dioxygenase (metapyrocatechase) from Pseudomonas putida mt-2. Struct Lond Engl 7:25–34. https://doi.org/10.1016/S0969-2126(99)80006-9
doi: 10.1016/S0969-2126(99)80006-9
LeGrand K, Petersen S, Zheng Y, Liu KK, Ozturk G, Chen JY, Young GM (2015) CsrA impacts survival of Yersinia enterocolitica by affecting a myriad of physiological activities. BMC Microbiol 15:31. https://doi.org/10.1186/s12866-015-0343-6
doi: 10.1186/s12866-015-0343-6
pubmed: 25885058
pmcid: 4336687
Mahaffey WR, Gibson DT, Cerniglia CE (1988) Bacterial oxidation of chemical carcinogens: formation of polycyclic aromatic acids from benz[a]anthracene. Appl Environ Microbiol 54:2415–2423. https://doi.org/10.1128/aem.54.10.2415-2423.1988
doi: 10.1128/aem.54.10.2415-2423.1988
pubmed: 2462407
pmcid: 204275
Moody JD, Freeman JP, Fu PP, Cerniglia CE (2004) Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 70(1):340–345. https://doi.org/10.1128/aem.70.1.340-345.2004
Mukherjee S, Yakhnin H, Kysela D, Sokoloski J, Babitzke P, Kearns DB (2011) CsrA-FliW interaction governs flagellin homeostasis and a checkpoint on flagellar morphogenesis in Bacillus subtilis. Mol Microbiol 82:447–461. https://doi.org/10.1111/j.1365-2958.2011.07822.x
doi: 10.1111/j.1365-2958.2011.07822.x
pubmed: 21895793
pmcid: 3192257
Mukherjee S, Babitzke P, Kearns DB (2013) FliW and FliS function independently to control cytoplasmic flagellin levels in Bacillus subtilis. J Bacteriol 195:297–306. https://doi.org/10.1128/JB.01654-12
doi: 10.1128/JB.01654-12
pubmed: 23144244
pmcid: 3553831
Pi H, Helmann JD (2018) Genome-wide characterization of the Fur Regulatory Network reveals a link between Catechol Degradation and Bacillibactin metabolism in Bacillus subtilis. mBio 9(5):e01451-18. https://doi.org/10.1128/mBio.01451-18
doi: 10.1128/mBio.01451-18
pubmed: 30377275
pmcid: 6212828
Porwal S, Lal S, Cheema S, Kalia VC (2009) Phylogeny in aid of the Present and Novel Microbial Lineages: diversity in Bacillus. PLOS ONE 4(2):E4438. https://doi.org/10.1371/journal.pone.0004438
doi: 10.1371/journal.pone.0004438
pubmed: 19212464
pmcid: 2639701
Qin W, Fan F, Zhu Y, Huang X, Ding A, Liu X, Dou J (2018) Anaerobic biodegradation of benzo(a)pyrene by a novel Cellulosimicrobium cellulans CWS2 isolated from polycyclic aromatic hydrocarbon-contaminated soil. Braz J Microbiol 49:258–268. https://doi.org/10.1016/j.bjm.2017.04.014
doi: 10.1016/j.bjm.2017.04.014
pubmed: 29102294
Rojas-Aparicio A, Hernández-Eligio JA, Toribio-Jiménez J, Rodríguez-Barrera MÁ, Castellanos-Escamilla M, Romero-Ramírez Y (2018) Genetic expression of pobA and fabHB in Bacillus licheniformis M2-7 in the presence of benzo[a]pyrene. Genet Mol Res 17(2): gmr16039916. https://doi.org/10.4238/gmr16039916
Romeo T, Babitzke P (2018) Global regulation by CsrA and its RNA antagonists. Microbiol Spectr 6(2). https://doi.org/10.1128/microbiolspec.RWR-0009-2017
Sambrook J, Green MR (2012) Molecular cloning: a laboratory manual, 4th ed. ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
doi: 10.1038/nprot.2008.73
pubmed: 18546601
Schneider J, Grosser R, Jayasimhulu K, Xue W, Warshawsky D (1996) Degradation of pyrene, benz[a]anthracene, and benzo[a]pyrene by Mycobacterium sp. strain RJGII-135, isolated from a former coal gasification site. Appl Environ Microbiol 62:13–19. https://doi.org/10.1128/aem.62.1.13-19.1996
doi: 10.1128/aem.62.1.13-19.1996
pubmed: 8572690
pmcid: 167768
Serrano-Angel LI, Segura D, Jimenez JT, Rodríguez-Barrera MA, Ortuño-Pineda C, Romero-Ramirez Y (2020) Carbon Storage Regulator A (csrA) Gene regulates motility and growth of Bacillus licheniformis in the Presence of Hydrocarbons. Microbiol Biotechnol Lett. 48:185–192. https://doi.org/10.4014/mbl.1909.09014
doi: 10.4014/mbl.1909.09014
Sim HW, Jung M, Ch YK (2013) Purification and characterization of protocatechuate 3,4-dioxygenase from Pseudomonas pseudoalcaligenes KF707. J Korean Soc Appl Biol Chem 56:401–408. https://doi.org/10.1007/s13765-013-3080-2
doi: 10.1007/s13765-013-3080-2
Song M, Luo C, Jiang L, Zhang D, Wang Y, Zhang G (2015) Identification of Benzo[a]pyrene-Metabolizing Bacteria in Forest Soils by using DNA-Based stable-isotope probing. Appl Environ Microbiol 81:7368–7376. https://doi.org/10.1128/AEM.01983-15
doi: 10.1128/AEM.01983-15
pubmed: 26253666
pmcid: 4592850
Sowada J, Schmalenberger A, Ebner I, Luch A, Tralau T (2014) Degradation of benzo[a]pyrene by bacterial isolates from human skin. FEMS Microbiol Ecol 88:129–139. https://doi.org/10.1111/1574-6941.12276
doi: 10.1111/1574-6941.12276
pubmed: 24372170
Tam LT, Eymann C, Albrecht D, Sietmann R, Schauer F, Hecker M, Antelmann H (2006) Differential gene expression in response to phenol and catechol reveals different metabolic activities for the degradation of aromatic compounds in Bacillus subtilis. Environ Microbiol 8(8):1408–1427. https://doi.org/10.1111/j.1462-2920.2006.01034.x
doi: 10.1111/j.1462-2920.2006.01034.x
pubmed: 16872404
Wang S, Yang F, Yang B (2017) Global effect of CsrA on gene expression in enterohemorrhagic Escherichia coli O157:H7. Res Microbiol 168:700–709. https://doi.org/10.1016/j.resmic.2017.08.003
doi: 10.1016/j.resmic.2017.08.003
pubmed: 28870757