Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Research Article

Heavy Metal Stress Tolerance by Serratia nematodiphila sp. MB307: Insights from Mass Spectrometry-based Proteomics

Author(s): Zarrin Basharat, Kyung-Mee Moon, Leonard J. Foster and Azra Yasmin*

Volume 19, Issue 5, 2022

Published on: 29 November, 2022

Page: [412 - 420] Pages: 9

DOI: 10.2174/1570164619666220617145437

Price: $65

Abstract

Background: Heavy metals impact living organisms deleteriously when they exceed the required limits. Their remediation by bacteria is a much-pursued area of environmental research. In this study, we explored the quantitative changes of four heavy metals (cadmium, chromium, zinc, copper), on the global and membrane proteome of gram-negative S. nematodiphila MB307. This is a versatile bacterium, isolated from the rhizosphere of heavy metal tolerating plant and equipped with characteristics ranging from useful biopeptide production to remediation of metals.

Methods: We explored changes in the static end products of coding DNA sequences, i.e., proteins after 24 incubation under metal stress, using LC-MS/MS. Data analysis was done using MaxQuant software coupled with the Perseus package.

Results: Up and downregulated protein fractions consisted prominently of chaperones, membrane integrity proteins, mobility or transporter proteins. Comparative analysis with previously studied bacteria and the functional contribution of these proteins to metal stress offer evidence for the survival of S. nematodiphila under high concentrations of selected metals.

Conclusion: The outcomes validate that this soil-derived bacterium is well attuned to removing these metals from the soil and water, and may be additionally useful for boosting the phytoremediation of metals. This study delivers interesting insights and overlays ground for further investigations on the mechanistic activity of this bacterium under pollutant stress.

Keywords: LC-MS/MS, metal pollution, proteome, remediation, bioinformatics, nematodiphila.

Graphical Abstract
[1]
Mishra, S.; Bharagava, R.N.; More, N.; Yadav, A.; Zainith, S.; Mani, S.; Chowdhary, P. Heavy metal contamination, an alarming threat to environment and human health. In: Environmental Biotechnology, For Sustainable Future; Springer: Singapore, 2019; pp. 103-125.
[http://dx.doi.org/10.1007/978-981-10-7284-0_5]
[2]
Mishra, S.; Bharagava, R.N. Toxic and genotoxic effects of hexavalent chromium in environment and its bioremediation strategies. J. Environ. Sci. Health Part C Environ. Carcinog. Ecotoxicol. Rev., 2016, 34(1), 1-32.
[http://dx.doi.org/10.1080/10590501.2015.1096883] [PMID: 26398402]
[3]
da Rocha, Junior, R.B.; Meira, H.M.; Almeida, D.G.; Rufino, R.D.; Luna, J.M.; Santos, V.A.; Sarubbo, L.A. Application of a low-cost bio-surfactant in heavy metal remediation processes. Biodegradation, 2019, 30(4), 215-233.
[http://dx.doi.org/10.1007/s10532-018-9833-1] [PMID: 29725781]
[4]
Selvi, A.; Rajasekar, A.; Theerthagiri, J.; Ananthaselvam, A.; Sathishkumar, K.; Madhavan, J.; Rahman, P.K. Integrated remediation pro-cesses toward heavy metal removal/recovery from various environments-a review. Front. Environ. Sci., 2019, 7, 66.
[http://dx.doi.org/10.3389/fenvs.2019.00066]
[5]
Basharat, Z. Genomic and Proteomic analysis of indigenous bacteria under the stress of selected micropollutants PhD dissertation; Fatima Jinnah Women University: Rawalpindi, Pakistan, 2018. prr.hec.gov.pk/jspui/handle/123456789/10274
[6]
Emenike, C.U.; Agamuthu, P.; Fauziah, S.H. Sustainable remediation of heavy metal polluted soil, A biotechnical interaction with selected bacteria species. J. Geochem. Explor., 2017, 182, 275-278.
[http://dx.doi.org/10.1016/j.gexplo.2016.10.002]
[7]
Kalita, D.; Joshi, S.R. Study on bioremediation of Lead by exopolysaccharide producing metallophilic bacterium isolated from extreme habitat. Biotechnol. Rep., 2017, 16, 48-57.
[http://dx.doi.org/10.1016/j.btre.2017.11.003] [PMID: 29167759]
[8]
Pires, C.; Franco, A.R.; Pereira, S.I.; Henriques, I.; Correia, A.; Magan, N.; Castro, P.M. Metal(loid)-contaminated soils as a source of culturable heterotrophic aerobic bacteria for remediation applications. Geomicrobiol. J., 2017, 34(9), 760-768.
[http://dx.doi.org/10.1080/01490451.2016.1261968]
[9]
Nwaehiri, U.L.; Akwukwaegbu, P.I.; Bright Nwoke, B.E. Bacterial remediation of heavy metal polluted soil and effluent from paper mill industry. Environ. Anal. Health Toxicol., 2020, 35(2), e2020009.
[http://dx.doi.org/10.5620/eaht.e2020009] [PMID: 32600007]
[10]
diCenzo, G.C.; Debiec, K.; Krzysztoforski, J.; Uhrynowski, W.; Mengoni, A.; Fagorzi, C.; Gorecki, A.; Dziewit, L.; Bajda, T.; Rzepa, G.; Drewniak, L. Genomic and biotechnological characterization of the heavy-metal resistant, arsenic-oxidizing bacterium Ensifer sp. M14. Genes, 2018, 9(8), 379.
[http://dx.doi.org/10.3390/genes9080379] [PMID: 30060533]
[11]
Huang, Y.; Wang, Y.; Feng, H.; Wang, J.; Yang, X.; Wang, Z. Genome-guided identification and characterization of bacteria for simultane-ous degradation of polycyclic aromatic hydrocarbons and resistance to hexavalent chromium. Int. Biodeterior. Biodegradation, 2019, 138, 78-86.
[http://dx.doi.org/10.1016/j.ibiod.2019.01.006]
[12]
Qin, W.; Zhao, J.; Yu, X.; Liu, X.; Chu, X.; Tian, J.; Wu, N. Improving Cadmium resistance in Escherichia coli through continuous ge-nome evolution. Front. Microbiol., 2019, 10, 278.
[http://dx.doi.org/10.3389/fmicb.2019.00278] [PMID: 30842762]
[13]
Lu, M.; Jiao, S.; Gao, E.; Song, X.; Li, Z.; Hao, X.; Rensing, C.; Wei, G. Transcriptome response to heavy metals in Sinorhizobium meliloti CCNWSX0020 reveals new metal resistance determinants that also promote bioremediation by Medicago lupulina in metal-contaminated Soil. Appl. Environ. Microbiol., 2017, 83(20), e01244-e17.
[http://dx.doi.org/10.1128/AEM.01244-17] [PMID: 28778889]
[14]
Gao, J.; Wu, S.; Liu, Y.; Wu, S.; Jiang, C.; Li, X.; Wang, R.; Bai, Z.; Zhuang, G.; Zhuang, X. Characterization and transcriptomic analysis of a highly Cr (VI)-resistant and-reductive plant-growth-promoting rhizobacterium Stenotrophomonas rhizophila DSM 14405T. Environ. Pollut., 2020, 263, 114622.
[http://dx.doi.org/10.1016/j.envpol.2020.114622]
[15]
Cheng, Z.; Wei, Y.Y.C.; Sung, W.W.; Glick, B.R.; McConkey, B.J. Proteomic analysis of the response of the plant growth-promoting bacte-rium Pseudomonas putida UW4 to nickel stress. Proteome Sci., 2009, 7(1), 18.
[http://dx.doi.org/10.1186/1477-5956-7-18] [PMID: 19422705]
[16]
Li, K.; Pidatala, V.R.; Shaik, R.; Datta, R.; Ramakrishna, W. Integrated metabolomic and proteomic approaches dissect the effect of metal-resistant bacteria on maize biomass and copper uptake. Environ. Sci. Technol., 2014, 48(2), 1184-1193.
[http://dx.doi.org/10.1021/es4047395] [PMID: 24383886]
[17]
Dhawi, F.; Datta, R.; Ramakrishna, W. Proteomics provides insights into biological pathways altered by plant growth promoting bacteria and Arbuscular mycorrhiza in sorghum grown in marginal soil. Biochim. Biophys. Acta. Proteins Proteomics, 2017, 1865(2), 243-251.
[http://dx.doi.org/10.1016/j.bbapap.2016.11.015] [PMID: 27913282]
[18]
Kumari, M.; Thakur, I.S. Biochemical and proteomic characterization of Paenibacillus sp. ISTP10 for its role in plant growth promotion and in rhizostabilization of cadmium. Bioresour. Technol. Rep., 2018, 3, 59-66.
[http://dx.doi.org/10.1016/j.biteb.2018.06.001]
[19]
Ma, L.; Xu, J.; Chen, N.; Li, M.; Feng, C. Microbial reduction fate of chromium (Cr) in aqueous solution by mixed bacterial consortium. Ecotoxicol. Environ. Saf., 2019, 170, 763-770.
[http://dx.doi.org/10.1016/j.ecoenv.2018.12.041] [PMID: 30583287]
[20]
Zhang, J.; Li, Q.; Zeng, Y.; Zhang, J.; Lu, G.; Dang, Z.; Guo, C. Bioaccumulation and distribution of cadmium by Burkholderia cepacia GYP1 under oligotrophic condition and mechanism analysis at proteome level. Ecotoxicol. Environ. Saf., 2019, 176, 162-169.
[http://dx.doi.org/10.1016/j.ecoenv.2019.03.091] [PMID: 30927637]
[21]
Al-Ghouti, M.A.; Abuqaoud, R.H.; Abu-Dieyeh, M.H. Detoxification of mercury pollutant leached from spent fluorescent lamps using bacterial strains. Waste Manag., 2016, 49, 238-244.
[http://dx.doi.org/10.1016/j.wasman.2015.12.013] [PMID: 26725036]
[22]
Basharat, Z.; Tanveer, F.; Yasmin, A.; Shinwari, Z.K.; He, T.; Tong, Y. Genome of Serratia nematodiphila MB307 offers unique insights into its diverse traits. Genome, 2018, 61(7), 469-476.
[http://dx.doi.org/10.1139/gen-2017-0250] [PMID: 29957088]
[23]
Haigh, R.; Kumar, B.; Sandrini, S.; Freestone, P. Mutation design and strain background influence the phenotype of Escherichia coli luxS mutants. Mol. Microbiol., 2013, 88(5), 951-969.
[http://dx.doi.org/10.1111/mmi.12237] [PMID: 23651217]
[24]
Sandrini, S.M.; Haigh, R.; Freestone, P.P. Fractionation by ultracentrifugation of gram negative cytoplasmic and membrane proteins. Bio Protoc., 2014, 4(21), e1287.
[http://dx.doi.org/10.21769/BioProtoc.1287]
[25]
Kruger, N.J. The Bradford method for protein quantitation. In: The protein protocols handbook; Humana Press: Totowa, NJ, 2009; pp. 17-24.
[http://dx.doi.org/10.1007/978-1-59745-198-7_4]
[26]
Ishihama, Y.; Rappsilber, J.; Andersen, J.S.; Mann, M. Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A, 2002, 979(1-2), 233-239.
[http://dx.doi.org/10.1016/S0021-9673(02)01402-4] [PMID: 12498253]
[27]
Squair, J.W.; Tigchelaar, S.; Moon, K.M.; Liu, J.; Tetzlaff, W.; Kwon, B.K.; Krassioukov, A.V.; West, C.R.; Foster, L.J.; Skinnider, M.A. Integrated systems analysis reveals conserved gene networks underlying response to spinal cord injury. eLife, 2018, 7, e39188.
[http://dx.doi.org/10.7554/eLife.39188] [PMID: 30277459]
[28]
Gayoso, C.M.; Mateos, J.; Méndez, J.A.; Fernández-Puente, P.; Rumbo, C.; Tomás, M.; Martínez de Ilarduya, O.; Bou, G. Molecular mechanisms involved in the response to desiccation stress and persistence in Acinetobacter baumannii. J. Proteome Res., 2014, 13(2), 460-476.
[http://dx.doi.org/10.1021/pr400603f] [PMID: 24299215]
[29]
Lacerda, C.M.; Choe, L.H.; Reardon, K.F. Metaproteomic analysis of a bacterial community response to cadmium exposure. J. Proteome Res., 2007, 6(3), 1145-1152.
[http://dx.doi.org/10.1021/pr060477v] [PMID: 17284062]
[30]
Park, S.; Ely, R.L. Candidate stress genes of Nitrosomonas europaea for monitoring inhibition of nitrification by heavy metals. Appl. Environ. Microbiol., 2008, 74(17), 5475-5482.
[http://dx.doi.org/10.1128/AEM.00500-08] [PMID: 18606795]
[31]
Khan, Z.; Rehman, A.; Nisar, M.A.; Zafar, S.; Zerr, I. Biosorption behavior and proteomic analysis of Escherichia coli P4 under cadmium stress. Chemosphere, 2017, 174, 136-147.
[http://dx.doi.org/10.1016/j.chemosphere.2017.01.132] [PMID: 28161514]
[32]
Chandrangsu, P.; Rensing, C.; Helmann, J.D. Metal homeostasis and resistance in bacteria. Nat. Rev. Microbiol., 2017, 15(6), 338-350.
[http://dx.doi.org/10.1038/nrmicro.2017.15] [PMID: 28344348]
[33]
Company, R.; Antúnez, O.; Cosson, R.P.; Serafim, A.; Shillito, B.; Cajaraville, M.; Bebianno, M.J.; Torreblanca, A. Protein expression profiles in Bathymodiolus azoricus exposed to cadmium. Ecotoxicol. Environ. Saf., 2019, 171, 621-630.
[http://dx.doi.org/10.1016/j.ecoenv.2019.01.031] [PMID: 30658297]
[34]
Ramos-Zúñiga, J.; Gallardo, S.; Martínez-Bussenius, C.; Norambuena, R.; Navarro, C.A.; Paradela, A.; Jerez, C.A. Response of the biomin-ing Acidithiobacillus ferrooxidans to high cadmium concentrations. J. Proteomics, 2019, 198, 132-144.
[http://dx.doi.org/10.1016/j.jprot.2018.12.013] [PMID: 30553947]
[35]
Chuanboon, K.; Na Nakorn, P.; Pannengpetch, S.; Laengsri, V.; Nuchnoi, P.; Isarankura-Na-Ayudhya, C.; Isarankura-Na-Ayudhya, P. Proteomics and bioinformatics analysis reveal potential roles of cadmium-binding proteins in cadmium tolerance and accumulation of En-terobacter cloacae. PeerJ, 2019, 7, e6904.
[http://dx.doi.org/10.7717/peerj.6904] [PMID: 31534833]
[36]
Kiliç, N.K.; Stensballe, A.; Otzen, D.E.; Dönmez, G. Proteomic changes in response to chromium(VI) toxicity in Pseudomonas aerugino-sa. Bioresour. Technol., 2010, 101(7), 2134-2140.
[http://dx.doi.org/10.1016/j.biortech.2009.11.008] [PMID: 19945860]
[37]
Thatheyus, A.J.; Ramya, D. Biosorption of chromium using bacteria, an overview. Sci. Int., 2016, 4(2), 74-79.
[http://dx.doi.org/10.17311/sciintl.2016.74.79]
[38]
Gang, H.; Xiao, C.; Xiao, Y.; Yan, W.; Bai, R.; Ding, R.; Yang, Z.; Zhao, F. Proteomic analysis of the reduction and resistance mechanisms of Shewanella oneidensis MR-1 under long-term hexavalent chromium stress. Environ. Int., 2019, 127, 94-102.
[http://dx.doi.org/10.1016/j.envint.2019.03.016] [PMID: 30909098]
[39]
Matilda, C.S.; Shanthi, C. Evaluation of suitability of primary growth models to fit bacterial growth under metal stress conditions. J. Pure Appl. Microbiol., 2016, 10(2), 1409-1415.
[40]
Dekker, L.; Arsène-Ploetze, F.; Santini, J.M. Comparative proteomics of Acidithiobacillus ferrooxidans grown in the presence and absence of uranium. Res. Microbiol., 2016, 167(3), 234-239.
[http://dx.doi.org/10.1016/j.resmic.2016.01.007] [PMID: 26829305]
[41]
Mugerfeld, I.; Law, B.A.; Wickham, G.S.; Thompson, D.K. A putative azoreductase gene is involved in the Shewanella oneidensis re-sponse to heavy metal stress. Appl. Microbiol. Biotechnol., 2009, 82(6), 1131-1141.
[http://dx.doi.org/10.1007/s00253-009-1911-1] [PMID: 19238379]
[42]
Stolyar, S.; He, Q.; Joachimiak, M.P.; He, Z.; Yang, Z.K.; Borglin, S.E.; Joyner, D.C.; Huang, K.; Alm, E.; Hazen, T.C.; Zhou, J.; Wall, J.D.; Arkin, A.P.; Stahl, D.A. Response of Desulfovibrio vulgaris to alkaline stress. J. Bacteriol., 2007, 189(24), 8944-8952.
[http://dx.doi.org/10.1128/JB.00284-07] [PMID: 17921288]
[43]
Hu, P.; Brodie, E.L.; Suzuki, Y.; McAdams, H.H.; Andersen, G.L. Whole-genome transcriptional analysis of heavy metal stresses in Cau-lobacter crescentus. J. Bacteriol., 2005, 187(24), 8437-8449.
[http://dx.doi.org/10.1128/JB.187.24.8437-8449.2005] [PMID: 16321948]
[44]
Marrero, J.; González, L.J.; Sánchez, A.; Ayala, M.; Paz-Lago, D.; González, W.; Fallarero, A.; Castellanos-Serra, L.; Coto, O. Effect of high concentration of Co (II) on Enterobacter liquefaciens strain C-1: A bacterium highly resistant to heavy metals with an unknown ge-nome. Proteomics, 2004, 4(5), 1265-1279.
[http://dx.doi.org/10.1002/pmic.200300735] [PMID: 15188394]
[45]
Eggers, C.T.; Murray, I.A.; Delmar, V.A.; Day, A.G.; Craik, C.S. The periplasmic serine protease inhibitor ecotin protects bacteria against neutrophil elastase. Biochem. J., 2004, 379(Pt 1), 107-118.
[http://dx.doi.org/10.1042/bj20031790] [PMID: 14705961]
[46]
Bonilla, J.O.; Callegari, E.A.; Estevéz, M.C.; Villegas, L.B. Intracellular Proteomic analysis of Streptomyces sp. MC1 when exposed to Cr (VI) by gel-Based and gel-Free methods. Curr. Microbiol., 2020, 77(1), 62-70.
[http://dx.doi.org/10.1007/s00284-019-01790-w] [PMID: 31705393]
[47]
Nandakumar, R.; Espirito Santo, C.; Madayiputhiya, N.; Grass, G. Quantitative proteomic profiling of the Escherichia coli response to metallic copper surfaces. Biometals, 2011, 24(3), 429-444.
[http://dx.doi.org/10.1007/s10534-011-9434-5] [PMID: 21384090]
[48]
Monchy, S.; Benotmane, M.A.; Wattiez, R.; van Aelst, S.; Auquier, V.; Borremans, B.; Mergeay, M.; Taghavi, S.; van der Lelie, D.; Val-laeys, T. Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology, 2006, 152(Pt 6), 1765-1776.
[http://dx.doi.org/10.1099/mic.0.28593-0] [PMID: 16735739]
[49]
Raivio, T.L.; Leblanc, S.K.; Price, N.L. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J. Bacteriol., 2013, 195(12), 2755-2767.
[http://dx.doi.org/10.1128/JB.00105-13] [PMID: 23564175]
[50]
Favre, L.; Ortalo-Magné, A.; Kerloch, L.; Pichereaux, C.; Misson, B.; Briand, J.F.; Garnier, C.; Culioli, G. Metabolomic and proteomic changes induced by growth inhibitory concentrations of copper in the biofilm-forming marine bacterium Pseudoalteromonas lipolytica. Metallomics, 2019, 11(11), 1887-1899.
[http://dx.doi.org/10.1039/C9MT00184K] [PMID: 31589240]
[51]
Hayyan, M.; Hashim, M.A.; AlNashef, I.M. Superoxide ion, generation and chemical implications. Chem. Rev., 2016, 116(5), 3029-3085.
[http://dx.doi.org/10.1021/acs.chemrev.5b00407] [PMID: 26875845]
[52]
Baker, J.; Sitthisak, S.; Sengupta, M.; Johnson, M.; Jayaswal, R.K.; Morrissey, J.A. Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. Appl. Environ. Microbiol., 2010, 76(1), 150-160.
[http://dx.doi.org/10.1128/AEM.02268-09] [PMID: 19880638]
[53]
Capdevila, D.A.; Wang, J.; Giedroc, D.P. Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface. J. Biol. Chem., 2016, 291(40), 20858-20868.
[http://dx.doi.org/10.1074/jbc.R116.742023] [PMID: 27462080]
[54]
Sukumaran, A.; Geddes-McAlister, J. Zinc limitation in Klebsiella pneumoniae profiled by quantitative proteomics influences transcrip-tional regulation and cation transporter-associated capsule production. BMC Microbiol., 2021, 21(1), 1-5.
[http://dx.doi.org/10.21203/rs.2.18241/v1]
[55]
Sharma, A.; Sharma, D.; Verma, S.K. Zinc binding proteome of a phytopathogen Xanthomonas translucens pv. undulosa. R. Soc. Open Sci., 2019, 6(9), 190369.
[http://dx.doi.org/10.1098/rsos.190369] [PMID: 31598288]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy