Genes That Enhance the Ecological Fitness of Shewanella Oneidensis MR-1 in Sediments Reveal the Value of Antibiotic Resistance

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2006 Nov 23

PMID 17114320

Citations 13

Authors

Jennifer L Groh

Qingwei Luo

Jimmy D Ballard

Lee R Krumholz

Affiliations

Soon will be listed here.

Abstract

Environmental bacteria persist in various habitats, yet little is known about the genes that contribute to growth and survival in their respective ecological niches. Signature-tagged mutagenesis (STM) of Shewanella oneidensis MR-1 coupled with a screen involving incubations of mutant strains in anoxic aquifer sediments allowed us to identify 47 genes that enhance fitness in sediments. Gene functions inferred from annotations provide us with insight into physiological and ecological processes that environmental bacteria use while growing in sediment ecosystems. Identification of the mexF gene and other potential membrane efflux components by STM demonstrated that homologues of multidrug resistance genes present in pathogens are required for sediment fitness of nonpathogenic bacteria. Further studies with a mexF deletion mutant demonstrated that the multidrug resistance pump encoded by mexF is required for resistance to antibiotics, including chloramphenicol and tetracycline. Chloramphenicol-adapted cultures exhibited mutations in the gene encoding a TetR family regulatory protein, indicating a role for this protein in regulating expression of the mexEF operon. The relative importance of mexF for sediment fitness suggests that antibiotic efflux may be a required process for bacteria living in sediment systems.

Citing Articles

Turning antagonists into allies: Bacterial-fungal interactions enhance the efficacy of controlling wilt disease.

Li T, Shi X, Wang J, Zhou Y, Wang T, Xu Y Sci Adv. 2025; 11(7):eads5089.

PMID: 39937904 PMC: 11817942. DOI: 10.1126/sciadv.ads5089.

Flux-Balance Analysis and Mobile CRISPRi-Guided Deletion of a Conditionally Essential Gene in MR-1.

Ford K, Kaste J, Shachar-Hill Y, TerAvest M ACS Synth Biol. 2022; 11(10):3405-3413.

PMID: 36219726 PMC: 9595118. DOI: 10.1021/acssynbio.2c00323.

Transcriptome analysis provides new insights into the tolerance and aerobic reduction of Shewanella decolorationis Ni1-3 to bromate.

Wang Y, Cai X, Fan J, Wang D, Mao Y Appl Microbiol Biotechnol. 2022; 106(12):4749-4761.

PMID: 35708750 DOI: 10.1007/s00253-022-12006-w.

The role of chemotaxis and efflux pumps on nitrate reduction in the toxic regions of a ciprofloxacin concentration gradient.

Alcalde R, Dundas C, Dong Y, Sanford R, Keitz B, Fouke B ISME J. 2021; 15(10):2920-2932.

PMID: 33927341 PMC: 8443623. DOI: 10.1038/s41396-021-00975-1.

Resistome, Mobilome and Virulome Analysis of and spp. Strains Isolated in Italian Aquaculture Centers.

Zago V, Veschetti L, Patuzzo C, Malerba G, Lleo M Microorganisms. 2020; 8(4).

PMID: 32326629 PMC: 7232470. DOI: 10.3390/microorganisms8040572.

References

Lomovskaya O, Lewis K . Emr, an Escherichia coli locus for multidrug resistance. Proc Natl Acad Sci U S A. 1992; 89(19):8938-42. PMC: 50039. DOI: 10.1073/pnas.89.19.8938. View

Poole K . Efflux-mediated antimicrobial resistance. J Antimicrob Chemother. 2005; 56(1):20-51. DOI: 10.1093/jac/dki171. View

Kohler T, Epp S, Curty L, Pechere J . Characterization of MexT, the regulator of the MexE-MexF-OprN multidrug efflux system of Pseudomonas aeruginosa. J Bacteriol. 1999; 181(20):6300-5. PMC: 103763. DOI: 10.1128/JB.181.20.6300-6305.1999. View

Shaw W, Brodsky R . Characterization of chloramphenicol acetyltransferase from chloramphenicol-resistant Staphylococcus aureus. J Bacteriol. 1968; 95(1):28-36. PMC: 251967. DOI: 10.1128/jb.95.1.28-36.1968. View

Beeman R, Suflita J . Environmental factors influencing methanogenesis in a shallow anoxic aquifer: a field and laboratory study. J Ind Microbiol. 1990; 5(1):45-57. DOI: 10.1007/BF01569605. View

Myers C, Nealson K . Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science. 1988; 240(4857):1319-21. DOI: 10.1126/science.240.4857.1319. View

Kennedy M, Lawless J . Role of chemotaxis in the ecology of denitrifiers. Appl Environ Microbiol. 1985; 49(1):109-14. PMC: 238353. DOI: 10.1128/aem.49.1.109-114.1985. View

Tseng T, Gratwick K, Kollman J, Park D, Nies D, Goffeau A . The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol. 2000; 1(1):107-25. View

Paulsen I . Multidrug efflux pumps and resistance: regulation and evolution. Curr Opin Microbiol. 2003; 6(5):446-51. DOI: 10.1016/j.mib.2003.08.005. View

10.

Schweizer H . Efflux as a mechanism of resistance to antimicrobials in Pseudomonas aeruginosa and related bacteria: unanswered questions. Genet Mol Res. 2003; 2(1):48-62. View

11.

Fukuda H, Hosaka M, Hirai K, Iyobe S . New norfloxacin resistance gene in Pseudomonas aeruginosa PAO. Antimicrob Agents Chemother. 1990; 34(9):1757-61. PMC: 171918. DOI: 10.1128/AAC.34.9.1757. View

12.

Tatusov R, Fedorova N, Jackson J, Jacobs A, Kiryutin B, Koonin E . The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003; 4:41. PMC: 222959. DOI: 10.1186/1471-2105-4-41. View

13.

DiChristina T, Moore C, Haller C . Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol. 2001; 184(1):142-51. PMC: 134750. DOI: 10.1128/JB.184.1.142-151.2002. View

14.

Gallert C, Fund K, Winter J . Antibiotic resistance of bacteria in raw and biologically treated sewage and in groundwater below leaking sewers. Appl Microbiol Biotechnol. 2005; 69(1):106-12. DOI: 10.1007/s00253-005-0033-7. View

15.

Chiang S, Mekalanos J . Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol Microbiol. 1998; 27(4):797-805. DOI: 10.1046/j.1365-2958.1998.00726.x. View

16.

Tikhonova E, Wang Q, Zgurskaya H . Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. J Bacteriol. 2002; 184(23):6499-507. PMC: 135444. DOI: 10.1128/JB.184.23.6499-6507.2002. View

17.

Lovley D, Phillips E . Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol. 1986; 51(4):683-9. PMC: 238947. DOI: 10.1128/aem.51.4.683-689.1986. View

18.

Herz K, Vimont S, Padan E, Berche P . Roles of NhaA, NhaB, and NhaD Na+/H+ antiporters in survival of Vibrio cholerae in a saline environment. J Bacteriol. 2003; 185(4):1236-44. PMC: 142861. DOI: 10.1128/JB.185.4.1236-1244.2003. View

19.

Lovley D, Chapelle F, Woodward J . Use of dissolved h2 concentrations to determine distribution of microbially catalyzed redox reactions in anoxic groundwater. Environ Sci Technol. 2011; 28(7):1205-10. DOI: 10.1021/es00056a005. View

20.

Wan X, VerBerkmoes N, McCue L, Stanek D, Connelly H, Hauser L . Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J Bacteriol. 2004; 186(24):8385-400. PMC: 532403. DOI: 10.1128/JB.186.24.8385-8400.2004. View