Effects of Exposure to the Herbicides, Glyphosate and Paraquat, on the Growth Inhibition and Antibiotic Susceptibility of Burkholderia pseudomallei
Keywords:
herbicides, antibiotic susceptibility, Burkholderia pseudomalleiAbstract
The emergence of antibiotic-resistant bacteria has increased due to selective pressure not just from antibiotics but also heavy metals, xenobiotic compounds and agrochemicals. Exposure to such compounds can induce genetic changes in bacteria which affect antibiotic susceptibility. In this study, we examined the effect of exposure to two herbicides, glyphosate and paraquat, on growth inhibition and antibiotic susceptibility of the soil bacterium Burkholderia pseudomallei.
B. pseudomallei is the cause of a frequently fatal infectious disease, melioidosis, and antibiotic resistant strains of this species can cause severe clinical and public health problems. Our results show that glyphosate and paraquat inhibit B. pseudomallei growth, with median minimum inhibitory concentrations (MICs) of 3.00 ± 0.00% (w v–1) for glyphosate and median MICs of 0.01 ± 0.00% (w v–1) to 0.04 ± 0.00% (w v–1) for paraquat. The MICs of ceftazidime (CAZ), doxycycline (DOX), trimethoprim (TMP), and sulfamethoxazole (SMX) against herbicide-treated and untreated B. pseudomallei were also determined. Glyphosate-treated and paraquat-treated B. pseudomallei were found to have decreased susceptibility to DOX and CAZ. Conversely, paraquat-treated B. pseudomallei became more susceptible to TMP. Taken together, these results show that exposure to glyphosate and paraquat inhibits B. pseudomallei growth and alters the bacterium’s antibiotic response. These observations demonstrate the impact of herbicides on an environmental microorganism of medical importance.
References
S.B. Levy, B. Marshall, Antibacterial resistance worldwide: causes, challenges and responses, Nat. Med. 10(S12) (2004) S122 – 129.
Y.-Y. Liu, Y. Wang, T.R. Walsh, L.-X. Yi, R. Zhang, J. Spencer, Y. Doi, G. Tian, B. Dong, X. Huang, L.-F. Yu, D. Gu, H. Ren, X. Chen, L. Lv, D. He, H. Zhou, Z. Liang, J.-H. Liu, J. Shen, Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study, Lancet Infect. Dis. 16(2) (2016) 161 – 168.
S.B. Levy, The Challenge of Antibiotic Resistance, Sci. Am. 278(3) (1998) 46 – 53.
B.M. Marshall, S.B. Levy, Food animals and antimicrobials: impacts on human health, Clin. Microbiol. Rev. 24(4) (2011) 718 – 733.
K. Chaianunporn, S. Tanuchit, S. Thammawat, T. Chaianunporn, Antibiotic resistance of environmental Isolates of Pseudomonas aeruginosa in Maha Sarakham province and Nong Bua Lamphu province, J. Sci. Technol. MSU. 35(2) (2016) 174 – 181.
A. Alonso, P. Sanchez, J.L. Martinez, Environmental selection of antibiotic resistance genes. Minireview, Environ. Microbiol. 3(1) (2001) 1 – 9.
K. Rangasamy, M. Athiappan, N. Devarajan, G. Samykannu, J.A. Parray, K.N. Aruljothi, N. Shameem, A.A. Alqarawi, A. Hashem, E.F. Abd_Allah, Pesticide degrading natural multidrug resistance bacterial flora, Microb. Pathog. 114 (2018) 304 – 310.
A.C. Cheng, B.J. Currie, Melioidosis: epidemiology, pathophysiology, and management, Clin. Microbiol. Rev. 18(2) (2005) 383 – 416.
D. Limmathurotsakul, S. Wongratanacheewin, N.P.J. Day, N. Teerawattanasook, W. Chaowagul, S. Chaisuksant, P. Chetchotisakd, S.J. Peacock, G. Wongsuvan, Increasing incidence of human melioidosis in northeast Thailand, Am. J. Trop. Med. Hyg. 82(6) (2010) 1113 – 1117.
S. Rattanavong, V. Wuthiekanun, S. Langla, P. Amornchai, J. Sirisouk, R. Phetsouvanh, C.E. Moore, S.J. Peacock, Y. Buisson, P.N. Newton, Randomized soil survey of the distribution of Burkholderia pseudomallei in rice fields in Laos, Appl. Environ. Microbiol. 77(2) (2011) 532 – 536.
B.J. Currie, D.A.B. Dance, A.C. Cheng, The global distribution of Burkholderia pseudomallei and melioidosis: an update, Trans. R. Soc. Trop. Med. Hyg. 102 (2008) S1 – 4.
S. Hinjoy, V. Hantrakun, S. Kongyu, J. Kaewrakmuk, T. Wangrangsimakul, S. Jitsuronk, W. Saengchun, S. Bhengsri, T. Akarachotpong, S. Thamthitiwat, O. Sangwichian, S. Anunnatsiri, R.W. Sermswan, G. Lertmemongkolchai, C.S. Tharinjaroen, K. Preechasuth, R. Udpaun, P. Chuensombut, N. Waranyasirikul, C. Anudit, S. Narenpitak, Y. Jutrakul, P. Teparrukkul, N. Teerawattanasook, K. Thanvisej, A. Suphan, P. Sukbut, K. Ploddi, P. Sirichotirat, B. Chiewchanyon, K. Rukseree, M. Hongsuwan, G. Wongsuwan, P. Sunthornsut, V. Wuthiekanun, S. Sachaphimukh, P. Wannapinij, W. Chierakul, C. Chewapreecha, J. Thaipadungpanit, N. Chantratita, S. Korbsrisate, A. Taunyok, S. Dunachie, P. Palittapongarnpim, S. Sirisinha, R. Kitphati, S. Iamsirithaworn, W. Chaowagul, P. Chetchotisak, T. Whistler, S. Wongratanacheewin, D. Limmathurotsakul, Melioidosis in Thailand: present and future, Trop. Med. Infect. Dis. 3(2) (2018) 38.
V. Wuthiekanun, D. Limmathurotsakul, N. Chantratita, E.J. Feil, N.P.J. Day, S.J. Peacock, Burkholderia pseudomallei is genetically diverse in agricultural land in northeast Thailand, PLoS Negl. Trop. Dis. 3(8) (2009) e496.
W.J. Wiersinga, B.J. Currie, S.J. Peacock, Melioidosis, N. Engl. J. Med. 367(11) (2012) 1035 – 1044.
T.J.J. Inglis, The treatment of melioidosis, Pharmaceuticals. 3(5) (2010) 1296 – 1303.
K.A. Rhodes, H.P. Schweizer, Antibiotic resistance in Burkholderia species, Drug Resist. Updat. 28 (2016) 82 – 90.
H.P. Schweizer, Mechanisms of antibiotic resistance in Burkholderia pseudomallei : implications for treatment of melioidosis, Future Microbiol. 7(12) (2012) 1389 – 1399.
V. Wuthiekanun, P. Amornchai, N. Saiprom, N. Chantratita, W. Chierakul, G.C.K.W. Koh, W. Chaowagul, N.P.J. Day, D. Limmathurotsakul, S.J. Peacock, Survey of antimicrobial resistance in clinical Burkholderia pseudomallei isolates over two decades in northeast Thailand, Antimicrob. Agents Chemother. 55(11) (2011) 5388 – 5391.
W. Chaowagul, N.J. White, D.A.B. Dance, Y. Wattanagoon, P. Naigowit, T.M.E. Davis, S. Looareesuwan, N. Pitakwatchara, Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand, J. Infect. Dis. 159(5) (1989) 890 – 899.
B. Kurenbach, D. Marjoshi, C.F. Amábile-Cuevas, G.C. Ferguson, W. Godsoe, P. Gibson, J.A. Heinemann, Sublethal exposure to commercial formulations of the herbicides dicamba, 2,4-dichlorophenoxyacetic acid, and glyphosate cause changes in antibiotic susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium, MBio. 6(2) (2015) e00009 – 15.
K. Chaianunporn, W. Chatuphonprasert, W. Mongkolthanaruk, T. Chaianunporn, Phytochemical analysis and effect of Senna alata leaf extract fractions on methicillin resistant Staphylococcus aureus and Pseudomonas aeruginosa, J. Sci. Technol. MSU. 37(2) (2018) 180 – 190.
B.Y. Reeks, F.R. Champlin, D.B. Paulsen, D.W. Scruggs, M.L. Lawrence, Effects of sub-minimum inhibitory concentration antibiotic levels and temperature on growth kinetics and outer membrane protein expression in Mannheimia haemolytica and Haemophilus somnus, Can. J. Vet. Res. Rev. Can. Rech. Veterinaire. 69(1) (2005) 1 – 10.
S.D. Sarker, L. Nahar, Y. Kumarasamy, Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals, Methods. 42(4) (2007) 321 – 324.
R.S. Fischer, A. Berry, C.G. Gaines, R.A. Jensen, Comparative action of glyphosate as a trigger of energy drain in eubacteria., J. Bacteriol. 168(3) (1986) 1147 – 1154.
R.M. Zablotowicz, K.N. Reddy, Impact of glyphosate on the symbiosis with glyphosate-resistant transgenic soybean, J. Environ. Qual. 33(3) (2004) 825 – 31.
M.H. Norris, Y. Kang, D. Lu, B.A. Wilcox, T.T. Hoang, Glyphosate resistance as a novel select-agent-compliant, non-antibiotic-selectable marker in chromosomal mutagenesis of the essential genes asd and dapB of Burkholderia pseudomallei, Appl. Environ. Microbiol. 75(19) (2009) 6062 – 6075.
J.M. Staub, L. Brand, M. Tran, Y. Kong, S.G. Rogers, Bacterial glyphosate resistance conferred by overexpression of an E. coli membrane efflux transporter, J. Ind. Microbiol. Biotechnol. 39(4) (2012) 641 – 647.
M. Kanehisa, M. Furumichi, M. Tanabe, Y. Sato, K. Morishima, KEGG: new perspectives on genomes, pathways, diseases and drugs, Nucleic Acids Res. 45(D1) (2017) D353 – 361.
J.A. Imlay, Pathways of oxidative damage, Annu. Rev. Microbiol. 57(1) (2003) 395 – 418.
M. Vanaporn, M. Wand, S.L. Michell, M. Sarkar-Tyson, P. Ireland, S. Goldman, C. Kewcharoenwong, D. Rinchai, G. Lertmemongkolchai, R.W. Titball, Superoxide dismutase C is required for intracellular survival and virulence of Burkholderia pseudomallei, Microbiology. 157(8) (2011) 2392 – 2400.
S.C. Grace, Phylogenetic distribution of superoxide dismutase supports an endosymbiotic origin for chloroplasts and mitochondria, Life Sci. 47(21) (1990) 1875 – 1886.
K.L.R. Dunn, J.L. Farrant, P.R. Langford, J.S. Kroll, Bacterial [Cu,Zn]-cofactored superoxide dismutase protects opsonized, encapsulated Neisseria meningitidis from phagocytosis by human monocytes/macrophages, Infect. Immun. 71(3) (2003) 1604 – 1607.
I.-H. Kang, J.S. Kim, J.K. Lee, The virulence of Vibrio vulnificus is affected by the cellular level of superoxide dismutase activity, J. Microbiol. Biotechnol. 17(8) (2007) 1399 – 1402.
K.E. Keith, M.A. Valvano, Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia, Infect. Immun. 75(5) (2007) 2451 – 2460.
M.R. Parsek, P.K. Singh, Bacterial biofilms: an emerging link to disease pathogenesis, Annu. Rev. Microbiol. 57 (2003) 677 – 701.
H.C. Flemming, J. Wingender, The biofilm matrix, Nat. Rev. Microbiol. 8(9) (2010) 623 – 633.
J.L. Rosner, Nonheritable resistance to chloramphenicol and other antibiotics induced by salicylates and other chemotactic repellents in Escherichia coli K-12., Proc. Natl. Acad. Sci. 82(24) (1985) 8771 – 8774.
W.H. Wang, Aspirin inhibits the growth of Helicobacter pylori and enhances its susceptibility to antimicrobial agents, Gut. 52(4) (2003) 490 – 495.
D. Du, Z. Wang, N.R. James, J.E. Voss, E. Klimont, T. Ohene-Agyei, H. Venter, W. Chiu, B.F. Luisi, Structure of the AcrAB–TolC multidrug efflux pump, Nature. 509(7501) (2014) 512 – 515.
M.N. Alekshun, S.B. Levy, The mar regulon: multiple resistance to antibiotics and other toxic chemicals, Trends Microbiol. 7(10) (1999) 410 – 413.
L. Fernandez, R.E.W. Hancock, Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance, Clin. Microbiol. Rev. 25(4) (2012) 661 – 681.
C. Bellé, S.M. Kulczynski, C.J. Basso, T. Edu Kaspary, F.P. Lamego, M.A.B. Pinto, Yield and quality of wheat seeds as a function of desiccation stages and herbicides, J. Seed Sci. 36(1) (2014) 63 – 70.
J.A.S. Moretto, L.M. Altarugio, P.A. Andrade, A.L. Fachin, F.D. Andreote, E.G. Stehling, Changes in bacterial community after application of three different herbicides, FEMS Microbiol. Lett. 364(13) (2017). 1 – 6.
C. Thiour-Mauprivez, F. Martin-Laurent, C. Calvayrac, L. Barthelmebs, Effects of herbicide on non-target microorganisms: towards a new class of biomarkers?, Sci. Total Environ. 684 (2019) 314 – 325.
C.F. Amábile-Cuevas, Antibiotic resistance: from Darwin to Lederberg to Keynes, Microb. Drug Resist. 19(2) (2013) 73 – 87.
F. Mauffrey, P.Y. Baccara, C. Gruffaz, S. Vuilleumier, G. Imfeld, Bacterial community composition and genes for herbicide degradation in a stormwater wetland collecting herbicide runoff, Water. Air. Soil Pollut. 228(12) (2017) 452.
M. Haeseker, L. Stol,, F. Nieman, C. Hoebe, C. Neef, C. Bruggeman, A. Verbon, The ciprofloxacin target AUC : MIC ratio is not reached in hospitalized patients with the recommended dosing regimens: ciprofloxacin concentrations in hospitalized patients, Br. J. Clin. Pharmacol. 75(1) (2013) 180 – 185.
A. Forrest, D.E. Nix, C.H. Ballow, T.F. Goss, M.C. Birmingham, J.J. Schentag, Pharmacodynamics of intravenous ciprofloxacin in seriously ill patients., Antimicrob. Agents Chemother. 37(5) (1993) 1073 – 1081.
R.J. Hassing, W.H.F. Goessens, D.J. Mevius, W. Pelt, J.W. Mouton, A. Verbon, P.J. Genderen, Decreased ciprofloxacin susceptibility in Salmonella Typhi and Paratyphi infections in ill-returned travellers: the impact on clinical outcome and future treatment options, Eur. J. Clin. Microbiol. Infect. Dis. 32(10) (2013) 1295 – 1301.
F. Baquero, Low-level antibacterial resistance: a gateway to clinical resistance, Drug Resist. Updat. 4(2) (2001) 93 – 105.
Z. Shen, X.Y. Pu, Q. Zhang, Salicylate functions as an efflux pump inducer and promotes the emergence of fluoroquinolone-resistant Campylobacter jejuni mutants, Appl. Environ. Microbiol. 77(20) (2011) 7128 – 7133.