Analysis of antibiotic resistance genes in Pseudomonas strains associated with plants: A computational investigation
DOI:
https://doi.org/10.15835/nsb14110938Keywords:
antibiotic resistance genes, in silico, plant-associated bacteria, PseudomonasAbstract
The species of the genus Pseudomonas are an important part of the microbiota associated with plants. These species can be beneficial to the host plant by promoting its growth, and by protecting it against diseases, but they can also have a phytopathogenic effect. The genus Pseudomonas and especially the species P. aeruginosa is classified among the pathogenic species, that are multi-resistant to antibiotics due to the possession of a large number of antibiotic resistance genes (ARGs). Therefore, the risk of contamination of crops by these genes is real and likely to present a danger in terms of human health. In this study, the genomic sequences of 21 strains of Pseudomonas associated with plants were in silico analyzed to assess the number and diversity of ARGs. A number of 63 ARGs belonging to seven different species were detected among the studied gnomes. The phylogenetic and the physicochemical properties of the proteins encoded by these genes were analyzed. The interaction network of the studied genes has been established; it shows great connectivity between the genes involved in the different systems of antibiotic efflux in Pseudomonas.
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Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, … McArthur AG (2020). CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Research 48:517-525. https://doi.org/10.1093/nar/gkz935
Armenteros JJA, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, … Nielsen H (2019). SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology 37:420-423. https://doi.org/10.1038/s41587-019-0036-z
Barbier F, Wolff M (2010). Multirésistance chez Pseudomonas aeruginosa. Vers l’impasse thérapeutique ? Multi-drug resistant Pseudomonas aeruginosa: towards a therapeutic dead end? Médecine/sciences (Paris) 26:960-968. https://doi.org/10.1051/medsci/20102611960
Beharry Z, Palzkill T (2005). Functional analysis of active site residues of the fosfomycin resistance enzyme FosA from Pseudomonas aeruginosa. Journal of Biological Chemistry 280(18):17786-17791. https://doi.org/10.1074/jbc.M501052200
Belimov AA, Dodd IC, Safronova VI, Hontzeas N, Davies WJ (2007). Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. Journal of Experimental Botany 58(6):1485-1495. https://doi.org/10.1093/jxb/erm010
Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, … Kreuzinger N (2015). Tackling antibiotic resistance: the environmental framework. Nature Reviews Microbiology 13:310-317. https://doi.org/10.1038/nrmicro3439
Boucher WH, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, … Bartlett J (2009). Bad bugs, No drugs: No ESKAPE! An update from the infectious diseases society of America. Clinical Infectious Diseases 48(1):1-12. https://doi.org/10.1086/595011
Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A (2017) Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annual Review of Phytopathology 55:61-83. https://doi.org/10.1146/annurev-phyto-080516-035641
Braz VS, Furlan JPR, Fernandes AFT, Stehling EG (2016). Mutations in NalC induce MexAB-OprM overexpression resulting in high level of aztreonam resistance in environmental isolates of Pseudomonas aeruginosa. FEMS Microbiology Letters. https://doi.org/10.1093/femsle/fnw166
Burrowes E, Baysse C, Adams C, O'Gara F (2006). Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152:405-418. https://doi.org/10.1099/mic.0.28324-0
Chuanchuen R, Murata T, Gotoh N, Schweizer HP (2005). Substrate-dependent utilization of OprM or OpmH by the Pseudomonas aeruginosa MexJK efflux pump. Antimicrobial Agents and Chemotherapy 49(5):2133-2136. https://doi.org/10.1128/aac.49.5.2133-2136.2005
Chuanchuen R, Narasaki C T, Schweizer HP (2002). The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan. Journal of Bacteriology 184:5036-5044. https://doi.org/10.1128/jb.184.18.5036-5044.2002
Coyne S, Courvalin P, Périchon B (2011). Efflux-mediated antibiotic resistance in Acinetobacter spp. Antimicrobial Agents and Chemotherapy 55(3):947-53. http://dx.doi.org/10.1128/AAC.01388-10
Ezadi F, Ardebili A, Mirnejad R (2019). Antimicrobial susceptibility testing for polymyxins: challenges, issues, and recommendations. Journal of Clinical Microbiology 57(4):e01390-18. https://doi.org/10.1128/jcm.01390-18
Fernández L, Jenssen H, Bains M, Wiegand I, Gooderham WJ, Hancock REW (2012). The two-component system CprRS senses cationic peptides and triggers adaptive resistance in Pseudomonas aeruginosa independently of ParRS. Antimicrobial Agents and Chemotherapy 56(12):6212-6222. https://dx.doi.org/10.1128%2FAAC.01530-12
Fernandez M, Porcel M, de la Torre J, Molina-Henares MA, Daddaoua A, Llamas MA, … Duque E (2015). Analysis of the pathogenic potential of nosocomial Pseudomonas putida strains. Frontiers in Microbiology 6:871. https://doi.org/10.3389/fmicb.2015.00871
Fonseca EL, Marin MA, Encinas F, Vicente ACP (2015). Full characterization of the integrative and conjugative element carrying the metallo-β-lactamase bla SPM-1 and bicyclomycin bcr1 resistance genes found in the pandemic Pseudomonas aeruginosa clone SP/ST277. Journal of Antimicrobial Chemotherapy 70(9):2547-2550. https://doi.org/10.1093/jac/dkv152
Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111. https://doi.org/10.1126/science.1220761
Gao R, Stock AM (2009). Biological insights from structures of two-component proteins. Annual Review of Microbiology 63:133-154. https://doi.org/10.1146/annurev.micro.091208.073214
Gilarranz R, Juan C, Castillo-Vera J, Chamizo FJ, Artiles F, Álamo I, Oliver A (2013) First detection in Europe of the metallo-β-lactamase IMP-15 in clinical strains of Pseudomonas putida and Pseudomonas aeruginosa. Clinical Microbiology and Infection 19(9):E424-7. https://doi.org/10.1111/1469-0691.12248
Girlich D, Naas T, Nordmann P (2004). Biochemical characterization of the naturally occurring oxacillinase OXA-50 of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 48(6):2043-2048. https://dx.doi.org/10.1128%2FAAC.48.6.2043-2048.2004
Hainrichson M, Yaniv O, Cherniavsky M, Nudelman I, Shallom-Shezifi D, Yaron S, Baasov T (2007). Overexpression and initial characterization of the chromosomal aminoglycoside 3′-O-phosphotransferase APH (3′)-IIb from Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 51(2):774-776. https://dx.doi.org/10.1128%2FAAC.01034-06
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, … Sessitsch A (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79:293-320. https://doi.org/10.1128/mmbr.00050-14
He GX, Kuroda T, Mima T, Morita Y, Mizushima T, Tsuchiya T (2004). An H (+)-coupled multidrug efflux pump, PmpM, a member of the MATE family of transporters, from Pseudomonas aeruginosa. Journal of Bacteriology 186(1):262-5. https://dx.doi.org/10.1128%2FJB.186.1.262-265.2004
Higgins PG, Fluit AC, Milatovic D, Verhoef J, Schmitz FJ (2003). Mutations in GyrA, ParC, MexR and NfxB in clinical isolates of Pseudomonas aeruginosa. International Journal of Antimicrobial Agents 21(5):409-13. https://doi.org/10.1016/S0924-8579(03)00009-8
Jagdalea S, Ahiwaleb S, Gajbhiyec M, Kapadnisa B (2019). Green approach to phytopathogen: Characterization of lytic bacteriophages of Pseudomonas sp., an etiology of the bacterial blight of pomegranate. Microbiology Research 228:126300. https://doi.org/10.1016/j.micres.2019.126300
Juncker AS, Willenbrock H, Von Heijne G, Nielsen H, Brunak S, Krogh A (2003). Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Science 12(8):1652-62. https://doi.org/10.1110/ps.0303703
Kominko H, Gorazda K, Wzorek Z, Wojtas K (2018). Sustainable Management of Sewage Sludge for the Production of Organo-Mineral Fertilizers. Waste and Biomass Valorization 9: 1817-1826. https://doi.org/10.1007/s12649-017-9942-9
Lally RD, Galbally P, Moreira AS, Spink J, Ryan D, Germaine KJ, Dowling DN (2017). Application of endophytic Pseudomonas fluorescens and a bacterial consortium to Brassica napus can increase plant height and biomass under greenhouse and field conditions. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2017.02193
Le-Minh N, Khan SJ, Drewes JE, Stuetz RM (2010). Fate of antibiotics during municipal water recycling treatment processes. Water Research 44(15):4295 323. https://doi.org/10.1016/j.watres.2010.06.020
Li B, Yang Y, Ma L, Ju F, Guo F, Tiedje JM, Zhang T (2015). Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME Journal 9(11): 2490-2502. https://doi.org/10.1038/ismej.2015.59
Lister PD, Wolter DJ, Hanson ND (2009). Antibacterial-resistant Pseudomonas aeruginosa: Clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clinical Microbiology Reviews 22(4):582-610. https://doi.org/10.1128/cmr.00040-09
Luczkiewicz A, Kotlarska E, Artichowicz W, Tarasewicz K, Fudala-Ksiazek S (2015). Antimicrobial resistance of Pseudomonas spp. isolated from wastewater and wastewater-impacted marine coastal zone. Environmental Science and Pollution Research 22:19823-19834. https://dx.doi.org/10.1007%2Fs11356-015-5098-y
Ma C, Chang G (2007). Structure of the multidrug resistance efflux transporter EmrE from Escherichia coli. Proceedings of the National Academy of Sciences of USA 101(9):2852-2857. https://doi.org/10.1073/pnas.0400137101
Malik M, Li L, Zhao X, Kerns RJ, Berger JM, Drlica K (2014). Lethal synergy involving bicyclomycin: an approach for reviving old antibiotics. Antimicrobial Agents and Chemotherapy 69(12):3227-3235. https://doi.org/10.1093/jac/dku285
Masuda N, Gotoh N, Ohya S, Nishino T (1996). Quantitative correlation between susceptibility and OprJ production in NfxB mutants of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 40(4):909-13. https://doi.org/10.1128/aac.40.4.909
Mazurier S, Merieau A, Bergeau D, Decoin V, Sperandio D, Crépin A, … Latour X (2015). Type III secretion system and virulence markers highlight similarities and differences between human- and plant-associated pseudomonads related to Pseudomonas fluorescens and P. putida. Applied and Environmental Microbiology 81(7):2579-2590. https://dx.doi.org/10.1128%2FAEM.04160-14
Mima T, Kohira N, Li Y, Sekiya H, Ogawa W, Kuroda T, Tsuchiya T (2009). Gene cloning and characteristics of the RND-type multidrug efflux pump MuxABC-OpmB possessing two RND components in Pseudomonas aeruginosa. Microbiology 155(11):3509-3517. https://doi.org/10.1099/mic.0.031260-0
Mima T, Joshi S, Gomez-Escalada M, Schweizer HP (2007). Identification and characterization of TriABC-OpmH, a triclosan efflux pump of Pseudomonas aeruginosa requiring two membrane fusion proteins. Journal of Bacteriology 189(21):7600-7609. https://dx.doi.org/10.1128%2FJB.00850-07
Moore ERB, Tindall BJ, Martins dos Santos VAP, Piere DH, Ramos JL, Palleroni NJ (2006). Nonmedical: Pseudomonas. Prokaryotes 6:646-670. http://doi.org/0.1007/0-387-30746-x_21
Mulcahy H, O'Callaghan J, O'Grady EP, Adams C, O'Gara F (2006). The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infection and Immunity 74(5):3012-3015. https://doi.org/10.1128/iai.74.5.3012-3015.2006
Muller C, Plésiat P, Jeannot K (2011). A two-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and β-lactams in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 55(3):1211-1221. https://doi.org/10.1128/aac.01252-10
Nehme D, Poole K (2007). Assembly of the MexAB-OprM multidrug pump of Pseudomonas aeruginosa: component interactions defined by the study of pump mutant suppressors. Journal of Bacteriology 189(17):6118-6127. https://dx.doi.org/10.1128%2FJB.00718-07
Noble RC, Overman SB (1994). Pseudomonas stutzeri infection: a review of hospital isolates a review of the literature. Diagnostic Microbiology and Infectious Disease 19:51-56. https://doi.org/10.1016/0732-8893(94)90051-5
Pan M, Wong CKC, Chu LM (2014). Distribution of antibiotics in wastewater-irrigated soils and their accumulation in vegetable crops in the Pearl River Delta, Southern China. Journal of Agricultural and Food Chemistry 62:11062-11069. https://doi.org/10.1021/jf503850v
Park W, Pen˜a-Llopis S, Lee Y, Demple B (2006). Regulation of superoxide stress in Pseudomonas putida KT2440 is different from the SoxR paradigm in Escherichia coli. Biochemical and Biophysical Research Communications 341(1):51-56. https://doi.org/10.1016/j.bbrc.2005.12.142
Pérez-Varela M, Corral J, Aranda J, Barbé J (2018). Functional characterization of AbaQ, a novel effluux pump mediating quinolone resistance in Acinetobacter Baumannii. Antimicrobial Agents and Chemotherapy 62. https://doi.org/10.1128/aac.00906-18
Richardot C, Juarez P, Jeannot K, Patry I, Plésiat P, Llanes C (2016). Amino acid substitutions account for most MexS alterations in clinical nfxC mutants of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 60(4):2302-2310. https://dx.doi.org/10.1128%2FAAC.02622-15
Rodriguez-Martinez JM, Poirel L, Nordmann P (2009). Extended-spectrum cephalosporinases in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 53(5):1766-1771. https://doi.org/10.1128/aac.01410-08
Rundell EA, Commodore N, Goodman AL, Kazmierczak BI (2020). A screen for antibiotic resistance determinants reveals a fitness cost of the flagellum in Pseudomonas aeruginosa. Journal of Bacteriology 202(6). https://doi.org/10.1128/jb.00682-19
Sakhtah H, Koyama L, Zhang Y, Morales DK, Fields BL, Price-Whelan A, … Dietrich LEP (2016). The Pseudomonas aeruginosa efflux pump MexGHI-OpmD transports a natural phenazine that controls gene expression and biofilm development. Proceedings of the National Academy of Sciences of USA 113(25):E3538-3547. https://doi.org/10.1073/pnas.1600424113
Sarris PF, Trantas EA, Mpalantinaki E, Ververidis F, Goumas DE (2012). Pseudomonas viridiflava, a multi host plant pathogen with significant genetic variation at the molecular level. PLoS One 7(4):e36090. https://doi.org/10.1371/journal.pone.0036090
Scholz P, Haring V, Wittmann-Liebold B, Ashman K, Bagdasarian M, Scherzinger E (1989). Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 75(2):271-288. https://doi.org/10.1016/0378-1119(89)90273-4
Schulze RJ, Komar J, Botte M, Allen WJ, Whitehouse S, Gold VAM, … Ian Collinson I (2014). Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG–SecDF–YajC–YidC. Proceedings of the National Academy of Sciences of USA 111:4844-4849. https://doi.org/10.1073/pnas.1315901111
Schweizer HP (2003). Efflux as a mechanism of resistance to antimicrobials in Pseudomonas aeruginosa and related bacteria: unanswered questions. Genetics and Molecular Research 2(1):48-62.
Seubert W (1960). Degradation of isoprenoid compounds by micro-organisms. I. Isolation and characterization of an isoprenoid-degrading bacterium, Pseudomonas citronellolis sp. Journal of Bacteriology 79(3):426-34. https://doi.org/10.1128/jb.79.3.426-434.1960
Sivasakthi S, Usharani GA, Saranraj P (2014). Biocontrol potentiality of plant growth promoting bacteria (PGPR)- Pseudomonas fluorescens and Bacillus subtilis. African Journal of Agricultural Research 9:1265-1277. https://doi.org/10.5897/AJAR2013.7914
Sobel ML, Hocquet D, Cao L, Plesiat P, Poole K (2005b). Mutations in PA3574 (nalD) lead to increased MexAB-OprM expression and multidrug resistance in laboratory and clinical isolates of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 49(5):1782-1786. https://dx.doi.org/10.1128%2FAAC.49.5.1782-1786.2005
Sobel ML, Neshat S, Poole K (2005a). Mutations in PA2491 (mexS) promote MexT-dependent mexEF-oprN expression and multidrug resistance in a clinical strain of Pseudomonas aeruginosa. Journal of Bacteriology 187:1246-1253. https://dx.doi.org/10.1128%2FJB.187.4.1246-1253.2005
Srikumar R, Paul C J, Poole K (2000). Influence of mutations in the mexR repressor gene on expression of the MexA-MexB-oprM multidrug efflux system of Pseudomonas aeruginosa. Journal of Bacteriology 182:1410-1414. https://doi.org/10.1128/jb.182.5.1410-1414.2000
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, … Mering CV (2019). STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research 47:D607-613. https://doi.org/10.1093/nar/gky1131
Tarkowski P, Vereecke D (2014). Threats and opportunities of plant pathogenic bacteria. Biotechnology Advances 32:215-229. https://doi.org/10.1016/j.biotechadv.2013.11.001
Tian ZX, Yi XX, Cho A, O’Gara F, Wang YP (2016). CpxR activates MexAB-OprM efflux pump expression and enhances antibiotic resistance in both laboratory and clinical nalB-type isolates of Pseudomonas aeruginosa. PLoS Pathogens 12(10):e1005932. https://doi.org/10.1371/journal.ppat.1005932
Vogne C, Aires JR, Bailly C, Hocquet D, Plesiat P (2004). Role of the multidrug efflux system MexXY in the emergence of moderate resistance to aminoglycosides among Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Antimicrobial Agents and Chemotherapy 48:1676-1680. https://dx.doi.org/10.1128%2FAAC.48.5.1676-1680.2004
Wang D, Seeve C, Pierson LS, Pierson EA (2013). Transcriptome profiling reveals links between ParS/ParR, MexEF-OprN, and quorum sensing in the regulation of adaptation and virulence in Pseudomonas aeruginosa. BMC Genomics 14:618. https://doi.org/10.1186/1471-2164-14-618
White PA, Stokes HW, Bunny KL, Hall RM (1999). Characterisation of a chloramphenicol acetyltransferase determinant found in the chromosome of Pseudomonas aeruginosa. FEMS Microbiology Letters 175(1):27-35. https://doi.org/10.1111/j.1574-6968.1999.tb13598.x
Wichmann F, Udikovic-Kolic N, Andrew S, Handelsman J (2014). Diverse antibioticresistance genes in dairy cow manure. American Society of Microbiology mBio 5:e01017-13. https://doi.org/10.1128/mbio.01017-13
Zhang HB, Zhou Y, Huang YJ, Wu LH, Liu XH, Luo YM (2016). Residues and risks of veterinary antibiotics in protected vegetable soils following application of different manures. Chemosphere 152:229-237. https://doi.org/10.1016/j.chemosphere.2016.02.111
Zhu B, Chenb Q, Chen S, Zhu YG (2016). Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced? Environment International 98:152-159. http://dx.doi.org/10.1016/j.envint.2016.11.001

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