Bacillus pumilus proteome changes in response to 2,4,6-trinitrotoluene-induced stress.
Degradation
Gram-positive bacteria
Nitroaromatics
Proteome
Journal
Biodegradation
ISSN: 1572-9729
Titre abrégé: Biodegradation
Pays: Netherlands
ID NLM: 9100834
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
25
05
2022
accepted:
08
08
2022
pubmed:
19
8
2022
medline:
22
10
2022
entrez:
18
8
2022
Statut:
ppublish
Résumé
2,4,6-Trinitrotoluene (TNT) is the most widely used nitroaromatic compound and is highly resistant to degradation. Most aerobic microorganisms reduce TNT to amino derivatives via formation of nitroso- and hydroxylamine intermediates. Although pathways of TNT degradation are well studied, proteomic analysis of TNT-degrading bacteria was done only for some individual Gram-negative strains. Here, we isolated a Gram-positive strain from TNT-contaminated soil, identified it as Bacillus pumilus using 16S rRNA sequencing, analyzed its growth, the level of TNT transformation, ROS production, and revealed for the first time the bacillary proteome changes at toxic concentration of TNT. The transformation of TNT at all studied concentrations (20-200 mg/L) followed the path of nitro groups reduction with the formation of 4-amino-2,6-dinitrotoluene. Hydrogen peroxide production was detected during TNT transformation. Comparative proteomic analysis of B. pumilus showed that TNT (200 mg/L) inhibited expression of 46 and induced expression of 24 proteins. Among TNT upregulated proteins are those which are responsible for the reductive pathway of xenobiotic transformation, removal of oxidative stress, DNA repair, degradation of RNA and cellular proteins. The production of ribosomal proteins, some important metabolic proteins and proteins involved in cell division are downregulated by this xenobiotic.
Identifiants
pubmed: 35980495
doi: 10.1007/s10532-022-09997-8
pii: 10.1007/s10532-022-09997-8
doi:
Substances chimiques
Trinitrotoluene
118-96-7
Proteome
0
RNA, Ribosomal, 16S
0
Xenobiotics
0
Hydrogen Peroxide
BBX060AN9V
Reactive Oxygen Species
0
Soil
0
Ribosomal Proteins
0
Hydroxylamines
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
593-607Subventions
Organisme : Russian Science Foundation
ID : Grant No 22-24-00036
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Alothman ZA, Bahkali AH, Elgorban AM, Al-Otaibi MS, Ghfar AA, Gabr SA, et al. (2020) Bioremediation of explosive TNT by Trichoderma viride. Molecules 25(6):1393. https://doi.org/10.3390/molecules25061393
doi: 10.3390/molecules25061393
pmcid: 7144562
Cabrera MÁ, Márquez SL, Quezada CP, Osorio MI, Castro-Nallar E, González-Nilo FD, Pérez-Donoso JM (2020) Biotransformation of 2,4,6-trinitrotoluene by Pseudomonas sp. TNT3 isolated from Deception island, Antarctica. Environ Pollut 262:113922. https://doi.org/10.1016/j.envpol.2020.113922
doi: 10.1016/j.envpol.2020.113922
pubmed: 32443190
Cherepnev GV, Velizhinskaya TA, Yakovleva GYu, Denivarova NA, Kurinenko BM (2007) Assessing the toxic effect of 2,4,6-trinitrotoluene on cells of Escherichia coli K12 by flow cytofluorometry. Microbiology 76(3): 331–335. https://doi.org/10.1134/S0026261707030101
doi: 10.1134/S0026261707030101
Cho Y-S, Lee B-U, Kahng H-Y, Oh K-H (2009) Comparative analysis of 2,4,6-trinitrotoluene (TNT)-induced cellular responses and proteomes in Pseudomonas sp. HK-6 in two types of media. J Microbiol 47(2):220–224. https://doi.org/10.1007/s12275-008-0108-0
doi: 10.1007/s12275-008-0108-0
pubmed: 19412608
Esteve-Nuñez A, Caballero A, Ramos JL (2001) Biological degradation of 2,4,6-trinitrotoluene. Microbiol Mol Biol Rev 65(3):333–352. https://doi.org/10.1128/MMBR.65.3.335-352.2001
doi: 10.1128/MMBR.65.3.335-352.2001
Heyno E, Innocenti G, Lemaire SD, Issakidis-Bourguet E, Krieger-Liszkay A (2014) Putative role of the malate valve enzyme NADP-malate dehydrogenase in H
doi: 10.1098/rstb.2013.0228
pubmed: 24591715
pmcid: 3949393
Ho E-M, Chang H-W, Kim S-I, Kahng H-Y, Oh K-H (2004) Analysis of TNT (2,4,6-trinitrotoluene)-inducible cellular responses and stress shock proteome in Stenotrophomonas sp. OK-5. Curr Microbiol 49(5):346–352. https://doi.org/10.1007/s00284-004-4322-7
doi: 10.1007/s00284-004-4322-7
pubmed: 15486709
Khan MI, Lee J, Yoo K, Kim S, Park J (2015) Improved TNT detoxification by starch addition in a nitrogen-fixing Methylophilus-dominant aerobic microbial consortium. J Hazard Mater 300:873–881. https://doi.org/10.1016/j.jhazmat.2015.08.032
doi: 10.1016/j.jhazmat.2015.08.032
pubmed: 26342802
Khilyas IV, Ziganshin AM, Pannier AJ, Gerlach R (2013) Effect of ferrihydrite on 2,4,6-trinitrotoluene biotransformation by an aerobic yeast. Biodeg 24(5):631–644. https://doi.org/10.1007/s10532-012-9611-4
doi: 10.1007/s10532-012-9611-4
pubmed: 23239085
Khilyas IV, Lochnit G, Ilinskaya ON (2017) Proteomic analysis of 2,4,6-trinitrotoluene degrading yeast Yarrowia lipolytica. Front Microbiol 8:A.2600. https://doi.org/10.3389/fmicb.2017.02600
doi: 10.3389/fmicb.2017.02600
Konovalova OA, Yakovleva GY, Steryakov OV, Trushin MV (2013) Scanning probe microscopy in the study of morphometric changes and physical parameters of Escherichia coli bacteria under the action of 2,4,6 - trinitrotoluene. World Appl Sci J 23(4):507–509. https://doi.org/10.5829/idosi.wasj.2013.23.04.13077
doi: 10.5829/idosi.wasj.2013.23.04.13077
Kurinenko BM, Yakovleva GY, Denivarova NA, Abreimova YV (2003) Specific toxic effects of 2,4,6-trinitrotoluene on Bacillus subtilis SK1. Appl Biochem Microbiol 39(3):275–8
doi: 10.1023/A:1023527611310
Kurinenko BM, Denivarova NA, Davydov RE, Yakovleva GYu (2007) Features of the toxic action of 2,4,6-trinitrotoluene on Escherichia coli K12. Appl Biochem Microbiol 43(1):52–56. https://doi.org/10.1134/S0003683807010097
doi: 10.1134/S0003683807010097
Liao H-Y, Chien C-C, Tang P, Chen C-C, Chen C-Y, Chen S-C (2018) The integrated analysis of transcriptome and proteome for exploring the biodegradation mechanism of 2,4,6-trinitrotoluene by Citrobacter sp. J Hazard Mater 349:79–90. https://doi.org/10.1016/j.jhazmat.2018.01.039
doi: 10.1016/j.jhazmat.2018.01.039
pubmed: 29414755
Lin H, Chena Z, Megharajc M, Naidu R (2013) Biodegradation of TNT using Bacillus mycoides immobilized in PVA-sodium alginate-kaolin. Appl Clay Sci 83:336–342. https://doi.org/10.1016/j.clay.2013.08.004
doi: 10.1016/j.clay.2013.08.004
Mercimek HA, Dincer S, Guzeldag G, Ozsavli A, Matyar F (2013) Aerobic biodegradation of 2,4,6-trinitrotoluene (TNT) by Bacillus cereus isolated from contaminated soil. Microb Ecol. 66(3):512–521. https://doi.org/10.1007/s00248-013-0248-6
doi: 10.1007/s00248-013-0248-6
pubmed: 23715804
Miczak A, Kaberdin VR, Wei CL, Lin-Chao S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci USA 93(9):3865–3869. https://doi.org/10.1073/pnas.93.9.3865
doi: 10.1073/pnas.93.9.3865
pubmed: 8632981
pmcid: 39450
Naumenko EA, Sibgatullina GV, Mukhitov AR, Rodionov AA, Ilinskaya ON, Naumova RP (2013) 2,4,6-Trinitrotoluene as a trigger of oxidative stress in Fagopyrum tataricum callus cells. Rus J Plant Physiol 60(3):404–410. https://doi.org/10.1134/S1021443713030102
doi: 10.1134/S1021443713030102
Naumenko EA, Ahlemeyer B, Baumgart-Vogt E (2017) Species-specific differences in peroxisome proliferation, catalase, and SOD2 upregulation as well as toxicity in human, mouse, and rat hepatoma cells induced by the explosive and environmental pollutant 2,4,6-trinitrotoluene. Environ Toxicol 32(3):989–1006. https://doi.org/10.1002/tox.22299
doi: 10.1002/tox.22299
pubmed: 27322098
Serrano-González MY, Chandra R, Castillo-Zacarias C, Robledo-Padilla F, Rostro-Alanis M, Parra-Saldivar R (2018) Biotransformation and degradation of 2,4,6-trinitrotoluene by microbial metabolism and their interaction. Defence Technol 14(2):151–164. https://doi.org/10.1016/j.dt.2018.01.004
doi: 10.1016/j.dt.2018.01.004
Smets BF, Yin H, Esteve-Nuñez A (2007) TNT biotransformation: when chemistry confronts mineralization. Appl Microbiol Biotechnol 76(2):267–277. https://doi.org/10.1007/s00253-007-1008-7
doi: 10.1007/s00253-007-1008-7
pubmed: 17534614
Solyanikova P, Robota IV, Mazur DM, Lebedev AT, Golovleva LA (2014) Application of Bacillus sp. strain VT-8 for decontamination of TNT-polluted sites. Microbiology 83(5):577–584. https://doi.org/10.1134/S0026261714050257
doi: 10.1134/S0026261714050257
Whitacre DM (2012) Reviews of environmental contamination and toxicology. Springer, New York. http://www.springer.com/gp/book/9781461414629 .
doi: 10.1007/978-1-4614-1463-6
Wijker RS, Bolotin J, Nishino SF, Spain JC, Hofstetter TB (2013) Using compound-specific isotope analysis to assess biodegradation of nitroaromatic explosives in the subsurface. Environ Sci Technol 47(13):6872–6883. https://doi.org/10.1021/es3051845
doi: 10.1021/es3051845
pubmed: 23547531
Williford CW Jr, Mark Bricka R (1999) Extraction of TNT from aggregate soil fractions. J Hazard Mater 66(1–2):1–13. https://doi.org/10.1016/S0304-3894(98)00214-3
doi: 10.1016/S0304-3894(98)00214-3
pubmed: 10379027
Wu CF, Xu XM, Zhu Q, Deng MC, Feng L, Peng J, et al. (2014)An effective method for the detoxification of cyanide-rich wastewater by Bacillus sp. CN-22. Appl Microbiol Biotechnol 98(8):3801–7. https://doi.org/10.1007/s00253-013-5433-5
doi: 10.1007/s00253-013-5433-5
pubmed: 24337345
Xu M, Liu D, Sun P, Li Y, Wu M, Liu W, et al. (2021) Degradation of 2,4,6-trinitrotoluene (TNT): involvement of protocatechuate 3,4-dioxygenase (P34O) in Buttiauxella sp. S19-1. Toxics 9(10):231. https://doi.org/10.3390/toxics9100231
doi: 10.3390/toxics9100231
pubmed: 34678927
pmcid: 8540567
Yang X, Lai JL, Li J, Zhang Y, Luo XG, Li ZG (2021) Biodegradation and physiological response mechanism of a bacterial strain to 2,4,6-trinitrotoluene contamination. Chemosphere 270:129280. https://doi.org/10.1016/j.chemosphere.2020.129280
doi: 10.1016/j.chemosphere.2020.129280
pubmed: 33418226
Yin H, Wood TK, Smets BF (2005) Reductive transformation of TNT by Escherichia coli: pathway description. Appl Microbiol Biotechnol 67(3):397–404. https://doi.org/10.1007/s00253-004-1736-x
doi: 10.1007/s00253-004-1736-x
pubmed: 15490158
Ziganshin AM, Gerlach R (2014) Pathways of 2,4,6-trinitrotoluene transformation by aerobic yeasts. In: Singh SN (ed) Biological remediation of explosive residues, environmental science and engineering. Springer, Cham, pp 301–311
Ziganshin AM, Ziganshina EE, Byrne J, Gerlach R, Struve E, Biktagirov T, et al. (2015) Fe(III) mineral reduction followed by partial dissolution and reactive oxygen species generation during 2,4,6-trinitrotoluene transformation by the aerobic yeast Yarrowia lipolytica. AMB Express 5:1–12. https://doi.org/10.1186/s13568-014-0094-z
doi: 10.1186/s13568-014-0094-z