Translating eco-evolutionary biology into therapy to tackle antibiotic resistance.
Journal
Nature reviews. Microbiology
ISSN: 1740-1534
Titre abrégé: Nat Rev Microbiol
Pays: England
ID NLM: 101190261
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
accepted:
19
04
2023
medline:
14
9
2023
pubmed:
20
5
2023
entrez:
19
5
2023
Statut:
ppublish
Résumé
Antibiotic resistance is currently one of the most important public health problems. The golden age of antibiotic discovery ended decades ago, and new approaches are urgently needed. Therefore, preserving the efficacy of the antibiotics currently in use and developing compounds and strategies that specifically target antibiotic-resistant pathogens is critical. The identification of robust trends of antibiotic resistance evolution and of its associated trade-offs, such as collateral sensitivity or fitness costs, is invaluable for the design of rational evolution-based, ecology-based treatment approaches. In this Review, we discuss these evolutionary trade-offs and how such knowledge can aid in informing combination or alternating antibiotic therapies against bacterial infections. In addition, we discuss how targeting bacterial metabolism can enhance drug activity and impair antibiotic resistance evolution. Finally, we explore how an improved understanding of the original physiological function of antibiotic resistance determinants, which have evolved to reach clinical resistance after a process of historical contingency, may help to tackle antibiotic resistance.
Identifiants
pubmed: 37208461
doi: 10.1038/s41579-023-00902-5
pii: 10.1038/s41579-023-00902-5
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
671-685Informations de copyright
© 2023. Springer Nature Limited.
Références
Baquero, F. et al. Evolutionary pathways and trajectories in antibiotic resistance. Clin. Microbiol. Rev. 34, e0005019 (2021).
pubmed: 34190572
Blount, Z. D., Lenski, R. E. & Losos, J. B. Contingency and determinism in evolution: replaying life’s tape. Science https://doi.org/10.1126/science.aam5979 (2018).
doi: 10.1126/science.aam5979
pubmed: 30409860
Hernando-Amado, S., Coque, T. M., Baquero, F. & Martinez, J. L. Defining and combating antibiotic resistance from One Health and Global Health perspectives. Nat. Microbiol. 4, 1432–1442 (2019).
pubmed: 31439928
Pinheiro, F., Warsi, O., Andersson, D. I. & Lässig, M. Metabolic fitness landscapes predict the evolution of antibiotic resistance. Nat. Ecol. Evol. 5, 677–687 (2021).
pubmed: 33664488
Pal, C., Papp, B. & Lazar, V. Collateral sensitivity of antibiotic-resistant microbes. Trends Microbiol. 23, 401–407 (2015).
pmcid: 5958998
pubmed: 25818802
Imamovic, L. & Sommer, M. O. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl Med. 5, 204ra132 (2013). This is one of the most thorough studies on collateral sensitivity networks in response to a large set of antibiotics.
pubmed: 24068739
Herencias, C. et al. Collateral sensitivity associated with antibiotic resistance plasmids. eLife https://doi.org/10.7554/eLife.65130 (2021). This article provides seminal information on collateral sensitivity associated with the acquisition of mobile antibiotic resistance genes.
doi: 10.7554/eLife.65130
pmcid: 7837676
pubmed: 33470194
Nichol, D. et al. Antibiotic collateral sensitivity is contingent on the repeatability of evolution. Nat. Commun. 10, 334 (2019).
pmcid: 6338734
pubmed: 30659188
Roemhild, R. & Andersson, D. I. Mechanisms and therapeutic potential of collateral sensitivity to antibiotics. PLoS Pathog. 17, e1009172 (2021).
pmcid: 7808580
pubmed: 33444399
Allison, K. R., Brynildsen, M. P. & Collins, J. J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473, 216–220 (2011). This article shows how priming bacterial metabolism may help to eliminate bacterial persisters by using antibiotics to which they did not respond.
pmcid: 3145328
pubmed: 21562562
Baquero, F. & Martinez, J. L. Interventions on metabolism: making antibiotic-susceptible bacteria. MBio https://doi.org/10.1128/mBio.01950-17 (2017).
doi: 10.1128/mBio.01950-17
pmcid: 5705924
pubmed: 29184022
Laborda, P., Alcalde-Rico, M., Chini, A., Martinez, J. L. & Hernando-Amado, S. Discovery of inhibitors of Pseudomonas aeruginosa virulence through the search for natural-like compounds with a dual role as inducers and substrates of efflux pumps. Env. Microbiol. https://doi.org/10.1111/1462-2920.15511 (2021).
doi: 10.1111/1462-2920.15511
Knoppel, A., Nasvall, J. & Andersson, D. I. Evolution of antibiotic resistance without antibiotic exposure. Antimicrob. Agents Chemother. https://doi.org/10.1128/aac.01495-17 (2017). This article shows that bacterial populations can acquire antibiotic resistance even in the absence of antibiotic selective pressure.
doi: 10.1128/aac.01495-17
pmcid: 5655081
pubmed: 28893783
Baquero, F. Causality in biological transmission: forces and energies. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.MTBP-0018-2016 (2018).
doi: 10.1128/microbiolspec.MTBP-0018-2016
pubmed: 30191806
Laxminarayan, R. Antibiotic effectiveness: balancing conservation against innovation. Science 345, 1299–1301 (2014).
pubmed: 25214620
Szybalski, W. & Bryson, V. Genetic studies on microbial cross resistance to toxic agents. I. Cross resistance of Escherichia coli to fifteen antibiotics. J. Bacteriol. 64, 489–499 (1952).
pmcid: 169383
pubmed: 12999676
Podnecky, N. L. et al. Conserved collateral antibiotic susceptibility networks in diverse clinical strains of Escherichia coli. Nat. Commun. 9, 3673 (2018). This article reports a wide study on the conservation of collateral sensitivity among a diverse set of clinical E. coli isolates.
pmcid: 6131505
pubmed: 30202004
Roemhild, R., Bollenbach, T. & Andersson, D. I. The physiology and genetics of bacterial responses to antibiotic combinations. Nat. Rev. Microbiol. 20, 478–490 (2022).
pubmed: 35241807
Lázár, V. et al. Antibiotic-resistant bacteria show widespread collateral sensitivity to antimicrobial peptides. Nat. Microbiol. 3, 718–731 (2018).
pmcid: 6544545
pubmed: 29795541
Barbosa, C., Beardmore, R., Schulenburg, H. & Jansen, G. Antibiotic combination efficacy (ACE) networks for a Pseudomonas aeruginosa model. PLoS Biol. 16, e2004356 (2018).
pmcid: 5945231
pubmed: 29708964
Munck, C., Gumpert, H. K., Wallin, A. I., Wang, H. H. & Sommer, M. O. Prediction of resistance development against drug combinations by collateral responses to component drugs. Sci. Transl Med. 6, 262ra156 (2014).
pmcid: 4503331
pubmed: 25391482
Jahn, L. J. et al. Compatibility of evolutionary responses to constituent antibiotics drive resistance evolution to drug pairs. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msab006 (2021).
doi: 10.1093/molbev/msab006
pmcid: 8097295
pubmed: 33480997
Imamovic, L. et al. Drug-driven phenotypic convergence supports rational treatment strategies of chronic infections. Cell 172, 121–134.e14 (2018). This article shows that phenotypic convergence displayed by different mutants can drive collateral sensitivity-based therapeutic strategies.
pmcid: 5766827
pubmed: 29307490
Kim, S., Lieberman, T. D. & Kishony, R. Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. Proc. Natl Acad. Sci. USA 111, 14494–14499 (2014).
pmcid: 4210010
pubmed: 25246554
Barbosa, C., Romhild, R., Rosenstiel, P. & Schulenburg, H. Evolutionary stability of collateral sensitivity to antibiotics in the model pathogen Pseudomonas aeruginosa. eLife https://doi.org/10.7554/eLife.51481 (2019).
doi: 10.7554/eLife.51481
pmcid: 6881144
pubmed: 31658946
Baym, M., Stone, L. K. & Kishony, R. Multidrug evolutionary strategies to reverse antibiotic resistance. Science 351, aad3292 (2016).
pmcid: 5496981
pubmed: 26722002
Barbosa, C. et al. Alternative evolutionary paths to bacterial antibiotic resistance cause distinct collateral effects. Mol. Biol. Evol. 34, 2229–2244 (2017). This article shows that replicate populations of the same bacterial strain can present different evolutionary pathways in the presence of antibiotics and substantial variations in collateral sensitivity.
pmcid: 5850482
pubmed: 28541480
Lazar, V. et al. Bacterial evolution of antibiotic hypersensitivity. Mol. Syst. Biol. 9, 700 (2013).
pmcid: 3817406
pubmed: 24169403
Lazar, V. et al. Genome-wide analysis captures the determinants of the antibiotic cross-resistance interaction network. Nat. Commun. 5, 4352 (2014).
pubmed: 25000950
Sørum, V. et al. Evolutionary instability of collateral susceptibility networks in ciprofloxacin-resistant clinical Escherichia coli strains. mBio 13, e0044122 (2022).
pubmed: 35862779
Hernando-Amado, S., Sanz-García, F. & Martínez, J. L. Antibiotic resistance evolution is contingent on the quorum-sensing response in Pseudomonas aeruginosa. Mol. Biol. Evol. 36, 2238–2251 (2019).
pubmed: 31228244
Vogwill, T., Kojadinovic, M. & MacLean, R. C. Epistasis between antibiotic resistance mutations and genetic background shape the fitness effect of resistance across species of Pseudomonas. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2016.0151 (2016).
doi: 10.1098/rspb.2016.0151
pmcid: 4971204
pubmed: 27466449
Card, K. J., Thomas, M. D., Graves, J. L. Jr, Barrick, J. E. & Lenski, R. E. Genomic evolution of antibiotic resistance is contingent on genetic background following a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.2016886118 (2021).
doi: 10.1073/pnas.2016886118
pmcid: 7865137
pubmed: 33441451
Gambello, M. J. & Iglewski, B. H. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol. 173, 3000–3009 (1991).
pmcid: 207884
pubmed: 1902216
Liakopoulos, A. et al. Allele-specific collateral and fitness effects determine the dynamics of fluoroquinolone resistance evolution. Proc. Natl Acad. Sci. USA 119, e2121768119 (2022).
pmcid: 9170170
pubmed: 35476512
Beckley, A. M. & Wright, E. S. Identification of antibiotic pairs that evade concurrent resistance via a retrospective analysis of antimicrobial susceptibility test results. Lancet Microbe 2, e545–e554 (2021).
pmcid: 8496867
pubmed: 34632433
Ma, Y. & Chua, S. L. No collateral antibiotic sensitivity by alternating antibiotic pairs. Lancet Microbe 3, e7 (2022).
pubmed: 35544116
Lopez-Causape, C., Cabot, G., Del Barrio-Tofino, E. & Oliver, A. The versatile mutational resistome of Pseudomonas aeruginosa. Front. Microbiol. 9, 685 (2018).
pmcid: 5897538
pubmed: 29681898
Hernando-Amado, S., Sanz-García, F. & Martínez, J. L. Rapid and robust evolution of collateral sensitivity in Pseudomonas aeruginosa antibiotic-resistant mutants. Sci. Adv. 6, eaba5493 (2020). This analysis of a set of antibiotic-resistant mutants of P. aeruginosa PA14 enables the identification of robust collateral sensitivity patterns associated with the use of ciprofloxacin.
pmcid: 7406369
pubmed: 32821825
Hernando-Amado, S., Laborda, P., Valverde José, R. & Martínez José, L. Mutational background influences P. aeruginosa ciprofloxacin resistance evolution but preserves collateral sensitivity robustness. Proc. Natl Acad. Sci. USA 119, e2109370119 (2022).
pmcid: 9169633
pubmed: 35385351
Hernando-Amado, S. et al. Rapid phenotypic convergence towards collateral sensitivity in clinical isolates of Pseudomonas aeruginosa presenting different genomic backgrounds. Microbiol. Spectr. 11, e0227622 (2022). This study shows that robust collateral sensitivity patterns associated with the use of ciprofloxacin emerge in clinical strains of P. aeruginosa having different genomic backgrounds and mutational resistomes.
pubmed: 36533961
Laborda, P., Martinez, J. L. & Hernando-Amado, S. Convergent phenotypic evolution towards fosfomycin collateral sensitivity of Pseudomonas aeruginosa antibiotic-resistant mutants. Microb. Biotechnol. https://doi.org/10.1111/1751-7915.13817 (2021). This article shows that different resistant mutants, selected by different antibiotics, present convergent collateral sensitivity to fosfomycin.
doi: 10.1111/1751-7915.13817
pmcid: 8867969
pubmed: 33960651
Roemhild, R., Linkevicius, M. & Andersson, D. I. Molecular mechanisms of collateral sensitivity to the antibiotic nitrofurantoin. PLoS Biol. 18, e3000612 (2020).
pmcid: 7004380
pubmed: 31986134
Laborda, P., Martínez, J. L. & Hernando-Amado, S. Evolution of habitat-dependent antibiotic resistance in Pseudomonas aeruginosa. Microbiol. Spectr. 10, e0024722 (2022).
pubmed: 35766499
Allen, R. C., Pfrunder-Cardozo, K. R. & Hall, A. R. Collateral sensitivity interactions between antibiotics depend on local abiotic conditions. mSystems 6, e0105521 (2021).
pubmed: 34846167
Rodriguez de Evgrafov, M. C., Faza, M., Asimakopoulos, K. & Sommer, M. O. A. Systematic investigation of resistance evolution to common antibiotics reveals conserved collateral responses across common human pathogens. Antimicrob. Agents Chemother. https://doi.org/10.1128/aac.01273-20 (2020).
doi: 10.1128/aac.01273-20
pmcid: 7927859
pubmed: 33106260
Apjok, G. et al. Limited evolutionary conservation of the phenotypic effects of antibiotic resistance mutations. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msz109 (2019).
doi: 10.1093/molbev/msz109
pmcid: 6657729
pubmed: 31058961
Hernando-Amado, S., Laborda, P. & Martínez, J. L. Tackling antibiotic resistance by inducing transient and robust collateral sensitivity. Nat. Commun. 14, 1723 (2023). This article shows that transient antibiotic resistance is associated with robust collateral sensitivity. Therefore, this trade-off can be exploited without the need to select antibiotic-resistant mutants.
pmcid: 10063638
pubmed: 36997518
van Duijn, P. J. et al. The effects of antibiotic cycling and mixing on antibiotic resistance in intensive care units: a cluster-randomised crossover trial. Lancet Infect. Dis. 18, 401–409 (2018).
pubmed: 29396000
Freihofer, P. et al. Nonmutational compensation of the fitness cost of antibiotic resistance in mycobacteria by overexpression of tlyA rRNA methylase. RNA 22, 1836–1843 (2016).
pmcid: 5113204
pubmed: 27698071
Shcherbakov, D. et al. Directed mutagenesis of Mycobacterium smegmatis 16S rRNA to reconstruct the in-vivo evolution of aminoglycoside resistance in Mycobacterium tuberculosis. Mol. Microbiol. 77, 830–840 (2010).
pubmed: 20545852
Durão, P., Trindade, S., Sousa, A. & Gordo, I. Multiple resistance at no cost: rifampicin and streptomycin a dangerous liaison in the spread of antibiotic resistance. Mol. Biol. Evol. 32, 2675–2680 (2015).
pmcid: 4576707
pubmed: 26130082
Olivares Pacheco, J., Alvarez-Ortega, C., Alcalde Rico, M. & Martinez, J. L. Metabolic compensation of fitness costs is a general outcome for antibiotic-resistant Pseudomonas aeruginosa mutants overexpressing efflux pumps. mBio 8, https://doi.org/10.1128/mBio.00500-17 (2017). This article provides evidence that fitness costs associated with the acquisition of resistance can be compensated for by metabolic rewiring.
Baquero, F. et al. Allogenous selection of mutational collateral resistance: old drugs select for new resistance within antibiotic families. Front. Microbiol. 12, 757833 (2021).
pmcid: 8569428
pubmed: 34745065
Nichol, D., Bonomo, R. A. & Scott, J. G. It’s too soon to pull the plug on antibiotic cycling. Lancet Infect. Dis. 18, 493 (2018). This article asserts that empirical evidence is not sufficient to validate the effectiveness of antibiotic cycling in reducing antibiotic resistance.
pubmed: 29695354
Andersson, D. I. & Hughes, D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260–271 (2010).
pubmed: 20208551
Dunai, A. et al. Rapid decline of bacterial drug-resistance in an antibiotic-free environment through phenotypic reversion. eLife https://doi.org/10.7554/eLife.47088 (2019). This article shows that decline of antibiotic resistance in the absence of selection is drug specific.
doi: 10.7554/eLife.47088
pmcid: 6707769
pubmed: 31418687
Hernando-Amado, S., Laborda, P., Valverde, J. R. & Martínez, J. L. Rapid decline of ceftazidime resistance in antibiotic-free and sublethal environments is contingent on genetic background. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msac049 (2022).
doi: 10.1093/molbev/msac049
pmcid: 8935207
pubmed: 35291010
Trindade, S. et al. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet. 5, e1000578 (2009).
pmcid: 2706973
pubmed: 19629166
Ward, H., Perron, G. G. & Maclean, R. C. The cost of multiple drug resistance in Pseudomonas aeruginosa. J. Evol. Biol. 22, 997–1003 (2009).
pubmed: 19298493
Salverda, M. L. et al. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7, e1001321 (2011).
pmcid: 3048372
pubmed: 21408208
Lopatkin, A. J. et al. Clinically relevant mutations in core metabolic genes confer antibiotic resistance. Science https://doi.org/10.1126/science.aba0862 (2021). This article shows that the mutation of metabolic genes may confer antibiotic resistance, providing a linkage between metabolism and resistance to antimicrobials.
doi: 10.1126/science.aba0862
pmcid: 8285040
pubmed: 33602825
Gil-Gil, T. & Martínez, J. L. Fosfomycin resistance evolutionary pathways of Stenotrophomonas maltophilia in different growing conditions. Int. J. Mol. Sci. https://doi.org/10.3390/ijms23031132 (2022).
doi: 10.3390/ijms23031132
pmcid: 9323910
pubmed: 35886841
Gil-Gil, T., Corona, F., Martinez, J. L. & Bernardini, A. The inactivation of enzymes belonging to the central carbon metabolism is a novel mechanism of developing antibiotic resistance. mSystems https://doi.org/10.1128/mSystems.00282-20 (2020).
doi: 10.1128/mSystems.00282-20
pmcid: 8534728
pubmed: 32487742
Zampieri, M. et al. Metabolic constraints on the evolution of antibiotic resistance. Mol. Syst. Biol. 13, 917 (2017). This study shows that growth under glycolytic or gluconeogenic conditions modifies antibiotic resistance trajectories. The acquisition of resistance modifies bacterial metabolism, rendering weaknesses in resistant strains.
pmcid: 5371735
pubmed: 28265005
Shewaramani, S. et al. Anaerobically grown Escherichia coli has an enhanced mutation rate and distinct mutational spectra. PLoS Genet. 13, e1006570 (2017).
pmcid: 5289635
pubmed: 28103245
Su, Y. B., Kuang, S. F., Peng, X. X. & Li, H. The depressed P cycle contributes to the acquisition of ampicillin resistance in Edwardsiella piscicida. J. Proteom. 212, 103562 (2020).
Balaban, N. Q. et al. Definitions and guidelines for research on antibiotic persistence. Nat. Rev. Microbiol. 17, 441–448 (2019).
pmcid: 7136161
pubmed: 30980069
Andersson, D. I., Nicoloff, H. & Hjort, K. Mechanisms and clinical relevance of bacterial heteroresistance. Nat. Rev. Microbiol. 17, 479–496 (2019).
pubmed: 31235888
Bjorkman, J., Nagaev, I., Berg, O. G., Hughes, D. & Andersson, D. I. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287, 1479–1482 (2000). This seminal work shows that fitness cost associated with antibiotic resistance is not merely a non-specific growth defect and that this cost, and the mutations compensating for it, are environment specific.
pubmed: 10688795
Scortti, M. et al. Coexpression of virulence and fosfomycin susceptibility in Listeria: molecular basis of an antimicrobial in vitro–in vivo paradox. Nat. Med. 12, 515–517 (2006).
pubmed: 16633349
Baquero, F., Lanza, V. F., Baquero, M. R., Del Campo, R. & Bravo-Vázquez, D. A. Microcins in Enterobacteriaceae: peptide antimicrobials in the eco-active intestinal chemosphere. Front. Microbiol. 10, 2261 (2019).
pmcid: 6795089
pubmed: 31649628
Wayne, L. G. & Sramek, H. A. Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 38, 2054–2058 (1994).
pmcid: 284683
pubmed: 7811018
Lin, P. L. et al. Metronidazole prevents reactivation of latent Mycobacterium tuberculosis infection in macaques. Proc. Natl Acad. Sci. USA 109, 14188–14193 (2012).
pmcid: 3435210
pubmed: 22826237
Chung, W. Y. et al. Exogenous metabolite feeding on altering antibiotic susceptibility in Gram-negative bacteria through metabolic modulation: a review. Metabolomics 18, 47 (2022).
pubmed: 35781167
Fortuin, S. & Soares, N. C. The integration of proteomics and metabolomics data paving the way for a better understanding of the mechanisms underlying microbial acquired drug resistance. Front. Med. 9, 849838 (2022).
Gardner, S. G., Marshall, D. D., Daum, R. S., Powers, R. & Somerville, G. A. Metabolic mitigation of Staphylococcus aureus vancomycin intermediate-level susceptibility. Antimicrob. Agents Chemother. https://doi.org/10.1128/AAC.01608-17 (2018).
doi: 10.1128/AAC.01608-17
pubmed: 29109158
Zhao, X. L. et al. Glutamine promotes antibiotic uptake to kill multidrug-resistant uropathogenic bacteria. Sci. Transl Med. 13, eabj0716 (2021).
pubmed: 34936385
Grézal, G. et al. Plasticity and stereotypic rewiring of the transcriptome upon bacterial evolution of antibiotic resistance. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msad020 (2023). This study shows that antibiotic-resistant E. coli mutants selected by different antibiotics display convergent transcriptomic changes, possibly through convergent regulatory rewiring of the multidrug transport system, which renders increased susceptibility to antimicrobial peptides.
doi: 10.1126/science.aba0862
pmcid: 9927579
pubmed: 36718533
Su, Y. B. et al. Pyruvate cycle increases aminoglycoside efficacy and provides respiratory energy in bacteria. Proc. Natl Acad. Sci. USA 115, E1578–E1587 (2018).
pmcid: 5816162
pubmed: 29382755
Arrieta-Ortiz, M. L. et al. Disrupting the ArcA regulatory network amplifies the fitness cost of tetracycline resistance in Escherichia coli. mSystems, 8, e0090422 (2022). This study shows how understanding metabolic changes associated with the acquisition of antibiotic resistance may enable the identification of a compound that hampers antibiotic resistance.
pubmed: 36537814
Vestergaard, M. et al. Inhibition of the ATP synthase eliminates the intrinsic resistance of Staphylococcus aureus towards polymyxins. mBio https://doi.org/10.1128/mBio.01114-17 (2017).
doi: 10.1128/mBio.01114-17
pmcid: 5587909
pubmed: 28874470
Kim, H. J. et al. Pharmacological perturbation of thiamine metabolism sensitizes Pseudomonas aeruginosa to multiple antibacterial agents. Cell Chem. Biol. 29, 1317–1324.e5 (2022).
pubmed: 35901793
Jiang, M. et al. Na
doi: 10.1128/mBio.02086-20
pmcid: 7683393
pubmed: 33203750
Ye, J. Z. et al. Identification and efficacy of glycine, serine and threonine metabolism in potentiating kanamycin-mediated killing of Edwardsiella piscicida. J. Proteom. 183, 34–44 (2018).
Peng, B. et al. Exogenous alanine and/or glucose plus kanamycin kills antibiotic-resistant bacteria. Cell Metab. 21, 249–262 (2015).
pubmed: 25651179
Campbell, C. et al. Accumulation of succinyl coenzyme a perturbs the methicillin-resistant Staphylococcus aureus (MRSA) succinylome and is associated with increased susceptibility to beta-lactam antibiotics. mBio 12, e0053021 (2021).
pubmed: 34182779
Furniss, R. C. D. et al. Breaking antimicrobial resistance by disrupting extracytoplasmic protein folding. eLife https://doi.org/10.7554/eLife.57974 (2022).
doi: 10.7554/eLife.57974
pmcid: 8863373
pubmed: 35025730
Linares, J. F. et al. The global regulator Crc modulates metabolism, susceptibility to antibiotics and virulence in Pseudomonas aeruginosa. Env. Microbiol. 12, 3196–3212 (2010).
Zhu, Y. et al. Genome-scale metabolic modeling of responses to polymyxins in Pseudomonas aeruginosa. GigaScience https://doi.org/10.1093/gigascience/giy021 (2018).
doi: 10.1093/gigascience/giy021
pmcid: 6324547
pubmed: 30247613
Heinemann, M., Kummel, A., Ruinatscha, R. & Panke, S. In silico genome-scale reconstruction and validation of the Staphylococcus aureus metabolic network. Biotechnol. Bioeng. 92, 850–864 (2005). This seminal work shows how the study of metabolic networks may provide information about the mechanisms of antibiotic resistance.
pubmed: 16155945
Rêgo, A. M. et al. Metabolic profiles of multidrug resistant and extensively drug resistant Mycobacterium tuberculosis unveiled by metabolomics. Tuberculosis 126, 102043 (2020).
pubmed: 33370646
Zampieri, M., Zimmermann, M., Claassen, M. & Sauer, U. Nontargeted metabolomics reveals the multilevel response to antibiotic perturbations. Cell Rep. 19, 1214–1228 (2017).
pubmed: 28494870
Martinez, J. L. et al. A global view of antibiotic resistance. FEMS Microbiol. Rev. 33, 44–65 (2009).
pubmed: 19054120
Sanz-García, F. et al. Coming from the wild: multidrug resistant opportunistic pathogens presenting a primary, not human-linked, environmental habitat. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22158080 (2021).
doi: 10.3390/ijms22158080
pmcid: 8347278
pubmed: 34360847
Fajardo, A. et al. The neglected intrinsic resistome of bacterial pathogens. PLoS ONE 3, e1619 (2008).
pmcid: 2238818
pubmed: 18286176
Martinez, J. L. Antibiotics and antibiotic resistance genes in natural environments. Science 321, 365–367 (2008).
pubmed: 18635792
Payie, K. G. & Clarke, A. J. Characterization of gentamicin 2′-N-acetyltransferase from Providencia stuartii: its use of peptidoglycan metabolites for acetylation of both aminoglycosides and peptidoglycan. J. Bacteriol. 179, 4106–4114 (1997).
pmcid: 179228
pubmed: 9209022
Henderson, T. A., Young, K. D., Denome, S. A. & Elf, P. K. AmpC and AmpH, proteins related to the class C beta-lactamases, bind penicillin and contribute to the normal morphology of Escherichia coli. J. Bacteriol. 179, 6112–6121 (1997).
pmcid: 179516
pubmed: 9324260
Santos, J. M., Lobo, M., Matos, A. P., De Pedro, M. A. & Arraiano, C. M. The gene bolA regulates dacA (PBP5), dacC (PBP6) and ampC (AmpC), promoting normal morphology in Escherichia coli. Mol. Microbiol. 45, 1729–1740 (2002).
pubmed: 12354237
Torrens, G. et al. Regulation of AmpC-driven β-lactam resistance in Pseudomonas aeruginosa: different pathways, different signaling. mSystems https://doi.org/10.1128/mSystems.00524-19 (2019).
doi: 10.1128/mSystems.00524-19
pmcid: 6890930
pubmed: 31796566
Bernat, B. A., Laughlin, L. T. & Armstrong, R. N. Fosfomycin resistance protein (FosA) is a manganese metalloglutathione transferase related to glyoxalase I and the extradiol dioxygenases. Biochemistry 36, 3050–3055 (1997).
pubmed: 9115979
Allocati, N., Federici, L., Masulli, M. & Di Ilio, C. Glutathione transferases in bacteria. FEBS J. 276, 58–75 (2009).
pubmed: 19016852
Kim, H. B., Park, C. H., Gavin, M., Jacoby, G. A. & Hooper, D. C. Cold shock induces qnrA expression in Shewanella algae. Antimicrob. Agents Chemother. 55, 414–416 (2011).
pubmed: 21078945
Blanco, P. et al. Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants. Microorganisms https://doi.org/10.3390/microorganisms4010014 (2016).
doi: 10.3390/microorganisms4010014
pmcid: 5029519
pubmed: 27681908
Vargas, P. et al. Plant flavonoids target Pseudomonas syringae pv. tomato DC3000 flagella and type III secretion system. Environ. Microbiol. Rep. 5, 841–850 (2013).
pubmed: 24249293
Garcia-Leon, G. et al. A function of SmeDEF, the major quinolone resistance determinant of Stenotrophomonas maltophilia, is the colonization of plant roots. Appl. Environ. Microbiol. 80, 4559–4565 (2014).
pmcid: 4148791
pubmed: 24837376
Lyu, M. et al. Structural basis of peptide-based antimicrobial inhibition of a resistance-nodulation-cell division multidrug efflux pump. Microbiol. Spectr. 10, e0299022 (2022).
pubmed: 36121287
Sanz-Garcia, F. et al. Mycobacterial aminoglycoside acetyltransferases: a little of drug resistance, and a lot of other roles. Front. Microbiol. 10, 46 (2019).
pmcid: 6363676
pubmed: 30761098
Duan, L., Yi, M., Chen, J., Li, S. & Chen, W. Mycobacterium tuberculosis EIS gene inhibits macrophage autophagy through up-regulation of IL-10 by increasing the acetylation of histone H3. Biochem. Biophys. Res. Commun. 473, 1229–1234 (2016).
pubmed: 27079235
Li, Y., Green, K. D., Johnson, B. R. & Garneau-Tsodikova, S. Inhibition of aminoglycoside acetyltransferase resistance enzymes by metal salts. Antimicrob. Agents Chemother. 59, 4148–4156 (2015).
pmcid: 4468725
pubmed: 25941215
Hitch, T. C. A. et al. Automated analysis of genomic sequences facilitates high-throughput and comprehensive description of bacteria. ISME Commun. 1, 16 (2021).
pmcid: 9723785
pubmed: 36732617
Forster, S. C. et al. A human gut bacterial genome and culture collection for improved metagenomic analyses. Nat. Biotechnol. 37, 186–192 (2019).
pmcid: 6785715
pubmed: 30718869
Neville, B. A., Forster, S. C. & Lawley, T. D. Commensal Koch’s postulates: establishing causation in human microbiota research. Curr. Opin. Microbiol. 42, 47–52 (2018).
pubmed: 29112885
Feehan, A. & Garcia-Diaz, J. Bacterial, gut microbiome-modifying therapies to defend against multidrug resistant organisms. Microorganisms https://doi.org/10.3390/microorganisms8020166 (2020).
doi: 10.3390/microorganisms8020166
pmcid: 7074682
pubmed: 31991615
Huddleston, J. R. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect. Drug Resist. 7, 167–176 (2014).
pmcid: 4073975
pubmed: 25018641
Hyun, J. et al. Faecal microbiota transplantation reduces amounts of antibiotic resistance genes in patients with multidrug-resistant organisms. Antimicrob. Resist. Infect. Control. 11, 20 (2022).
pmcid: 8800327
pubmed: 35093183
Millan, B. et al. Fecal microbial transplants reduce antibiotic-resistant genes in patients with recurrent Clostridium difficile infection. Clin. Infect. Dis. 62, 1479–1486 (2016). The article provides information on the use of microbiome transplantation for fighting infections by highly resistant bacteria.
pmcid: 4885654
pubmed: 27025836
Leo, S. et al. Metagenomic characterization of gut microbiota of carriers of extended-spectrum beta-lactamase or carbapenemase-producing Enterobacteriaceae following treatment with oral antibiotics and fecal microbiota transplantation: results from a multicenter randomized trial. Microorganisms https://doi.org/10.3390/microorganisms8060941 (2020).
doi: 10.3390/microorganisms8060941
pmcid: 7357103
pubmed: 32585945
Singh, R. et al. Fecal microbiota transplantation against intestinal colonization by extended spectrum beta-lactamase producing Enterobacteriaceae: a proof of principle study. BMC Res. Notes 11, 190 (2018).
pmcid: 5863815
pubmed: 29566738
DeFilipp, Z. et al. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N. Engl. J. Med. 381, 2043–2050 (2019).
pubmed: 31665575
Lesbros-Pantoflickova, D., Corthesy-Theulaz, I. & Blum, A. L. Helicobacter pylori and probiotics. J. Nutr. 137, 812S–818S (2007).
pubmed: 17311980
Lin, Y. C. et al. Probiotic Bacillus affects Enterococcus faecalis antibiotic resistance transfer by interfering with pheromone signaling cascades. Appl. Environ. Microbiol. 87, e00442-21 (2021).
pmcid: 8316027
pubmed: 33893118
Lazdins, A. et al. Potentiation of curing by a broad-host-range self-transmissible vector for displacing resistance plasmids to tackle AMR. PLoS ONE 15, e0225202 (2020).
pmcid: 6961859
pubmed: 31940351
Wieers, G. et al. Do probiotics during in-hospital antibiotic treatment prevent colonization of gut microbiota with multi-drug-resistant bacteria? A randomized placebo-controlled trial comparing Saccharomyces to a mixture of Lactobacillus, Bifidobacterium, and Saccharomyces. Front. Public Health 8, 578089 (2020).
pubmed: 33763399
Ouwehand, A. C., Forssten, S., Hibberd, A. A., Lyra, A. & Stahl, B. Probiotic approach to prevent antibiotic resistance. Ann. Med. 48, 246–255 (2016).
pubmed: 27092975
Gueimonde, M., Sanchez, B., de Los Reyes-Gavilán, C. G. & Margolles, A. Antibiotic resistance in probiotic bacteria. Front. Microbiol. 4, 202 (2013).
pmcid: 3714544
pubmed: 23882264
Esaiassen, E. et al. Bifidobacterium longum subspecies infantis bacteremia in 3 extremely preterm infants receiving probiotics. Emerg. Infect. Dis. 22, 1664–1666 (2016).
pmcid: 4994345
pubmed: 27532215
Dharmaratne, P., Rahman, N., Leung, A. & Ip, M. Is there a role of faecal microbiota transplantation in reducing antibiotic resistance burden in gut? A systematic review and meta-analysis. Ann. Med. 53, 662–681 (2021).
pmcid: 8238059
pubmed: 34170204
Cavallo, F. M., Jordana, L., Friedrich, A. W., Glasner, C. & van Dijl, J. M. Bdellovibrio bacteriovorus: a potential ‘living antibiotic’ to control bacterial pathogens. Crit. Rev. Microbiol. 47, 630–646 (2021).
pubmed: 33934682
Perez, J., Contreras-Moreno, F. J., Marcos-Torres, F. J., Moraleda-Munoz, A. & Munoz-Dorado, J. The antibiotic crisis: how bacterial predators can help. Comput. Struct. Biotechnol. J. 18, 2547–2555 (2020).
pmcid: 7522538
pubmed: 33033577
Saralegui, C. et al. Strain-specific predation of Bdellovibrio bacteriovorus on Pseudomonas aeruginosa with a higher range for cystic fibrosis than for bacteremia isolates. Sci. Rep. 12, 10523 (2022).
pmcid: 9217795
pubmed: 35732651
Snyder, A. R., Williams, H. N., Baer, M. L., Walker, K. E. & Stine, O. C. 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int. J. Syst. Evol. Microbiol. 52, 2089–2094 (2002).
pubmed: 12508873
Atterbury, R. J. & Tyson, J. Predatory bacteria as living antibiotics — where are we now? Microbiology https://doi.org/10.1099/mic.0.001025 (2021). This article is a recent review on the potential use of bacterial predators for fighting infections.
doi: 10.1099/mic.0.001025
pubmed: 33465024
Bratanis, E., Andersson, T., Lood, R. & Bukowska-Faniband, E. Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes. Front. Microbiol. 11, 662 (2020).
pmcid: 7174725
pubmed: 32351487
Im, H., Choi, S. Y., Son, S. & Mitchell, R. J. Combined application of bacterial predation and violacein to kill polymicrobial pathogenic communities. Sci. Rep. 7, 14415 (2017).
pmcid: 5663959
pubmed: 29089523
Marine, E., Milner, D. S., Lambert, C., Sockett, R. E. & Pos, K. M. A novel method to determine antibiotic sensitivity in Bdellovibrio bacteriovorus reveals a DHFR-dependent natural trimethoprim resistance. Sci. Rep. 10, 5315 (2020).
pmcid: 7093396
pubmed: 32210253
Bornier, F. et al. Environmental free-living amoebae can predate on diverse antibiotic-resistant human pathogens. Appl. Environ. Microbiol. 87, e0074721 (2021).
pubmed: 34232736
Pérez-Acevedo, G., Bosch-Alcaraz, A. & Torra-Bou, J. E. Larval therapy for treatment of chronic wounds colonized by multi-resistant pathogens in a pediatric patient: a case study. J. Wound Ostomy Cont. Nurs. 49, 373–378 (2022).
Negus, D. et al. Predator versus pathogen: how does predatory Bdellovibrio bacteriovorus interface with the challenges of killing gram-negative pathogens in a host setting? Annu. Rev. Microbiol. 71, 441–457 (2017).
pubmed: 28886689
Sanchez, P. et al. Fitness of in vitro selected Pseudomonas aeruginosa nalB and nfxB multidrug resistant mutants. J. Antimicrob. Chemother. 50, 657–664 (2002).
pubmed: 12407121
Merker, M. et al. Evolutionary approaches to combat antibiotic resistance: opportunities and challenges for precision medicine. Front. Immunol. 11, 1938 (2020).
pmcid: 7481325
pubmed: 32983122
Di Venanzio, G. et al. Multidrug-resistant plasmids repress chromosomally encoded T6SS to enable their dissemination. Proc. Natl Acad. Sci. USA 116, 1378–1383 (2019).
pmcid: 6347727
pubmed: 30626645
Banerji, A., Jahne, M., Herrmann, M., Brinkman, N. & Keely, S. Bringing community ecology to bear on the issue of antimicrobial resistance. Front. Microbiol. 10, 2626 (2019).
pmcid: 6872637
pubmed: 31803161
Bottery, M. J. et al. Inter-species interactions alter antibiotic efficacy in bacterial communities. ISME J. 16, 812–821 (2022).
pubmed: 34628478
Adamowicz, E. M., Muza, M., Chacon, J. M. & Harcombe, W. R. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLoS Pathog. 16, e1008700 (2020).
pmcid: 7392344
pubmed: 32687537
Flynn, J. M. et al. Disruption of cross-feeding inhibits pathogen growth in the sputa of patients with cystic fibrosis. mSphere https://doi.org/10.1128/mSphere.00343-20 (2020).
doi: 10.1128/mSphere.00343-20
pmcid: 7193046
pubmed: 32350096
O’Brien, S., Baumgartner, M. & Hall, A. R. Species interactions drive the spread of ampicillin resistance in human-associated gut microbiota. Evol. Med. Public Health 9, 256–266 (2021).
pmcid: 8385247
pubmed: 34447576
Baumgartner, M., Bayer, F., Pfrunder-Cardozo, K. R., Buckling, A. & Hall, A. R. Resident microbial communities inhibit growth and antibiotic-resistance evolution of Escherichia coli in human gut microbiome samples. PLoS Biol. 18, e3000465 (2020).
pmcid: 7192512
pubmed: 32310938
Alcalde-Rico, M., Hernando-Amado, S., Blanco, P. & Martinez, J. L. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front. Microbiol. 7, 1483 (2016).
pmcid: 5030252
pubmed: 27708632
Wang-Kan, X. et al. Lack of AcrB efflux function confers loss of virulence on Salmonella enterica serovar Typhimurium. mBio https://doi.org/10.1128/mBio.00968-17 (2017).
doi: 10.1128/mBio.00968-17
pmcid: 5516257
pubmed: 28720734
Warner, D. M., Folster, J. P., Shafer, W. M. & Jerse, A. E. Regulation of the MtrC-MtrD-MtrE efflux-pump system modulates the in vivo fitness of Neisseria gonorrhoeae. J. Infect. Dis. 196, 1804–1812 (2007).
pubmed: 18190261
Palmer, A. C. & Kishony, R. Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nat. Rev. Genet. 14, 243–248 (2013).
pmcid: 3705945
pubmed: 23419278
Garcia-Leon, G., Salgado, F., Oliveros, J. C., Sanchez, M. B. & Martinez, J. L. Interplay between intrinsic and acquired resistance to quinolones in Stenotrophomonas maltophilia. Env. Microbiol. 16, 1282–1296 (2014).
Finney-Manchester, S. P. & Maheshri, N. Harnessing mutagenic homologous recombination for targeted mutagenesis in vivo by TaGTEAM. Nucleic Acids Res. 41, e99 (2013).
pmcid: 3643572
pubmed: 23470991
Ma, L. et al. CRISPR-Cas9-mediated saturated mutagenesis screen predicts clinical drug resistance with improved accuracy. Proc. Natl Acad. Sci. USA 114, 11751–11756 (2017).
pmcid: 5676903
pubmed: 29078326
Nyerges, A. et al. Directed evolution of multiple genomic loci allows the prediction of antibiotic resistance. Proc. Natl Acad. Sci. USA 115, E5726–E5735 (2018).
pmcid: 6016788
pubmed: 29871954
Álvarez, B., Mencía, M., de Lorenzo, V. & Fernández, L. In vivo diversification of target genomic sites using processive base deaminase fusions blocked by dCas9. Nat. Commun. 11, 6436 (2020).
pmcid: 7755918
pubmed: 33353963
O’Neill, A. J. & Chopra, I. Use of mutator strains for characterization of novel antimicrobial agents. Antimicrob. Agents Chemother. 45, 1599–1600 (2001).
pmcid: 90517
pubmed: 11372639
Sanz-García, F., Hernando-Amado, S. & Martínez, J. L. Mutation-driven evolution of Pseudomonas aeruginosa in the presence of either ceftazidime or ceftazidime-avibactam. Antimicrob. Agents Chemother. https://doi.org/10.1128/aac.01379-18 (2018).
doi: 10.1128/aac.01379-18
pmcid: 6153820
pubmed: 30082283
La Rosa, R., Rossi, E., Feist, A. M., Johansen, H. K. & Molin, S. Compensatory evolution of Pseudomonas aeruginosa’s slow growth phenotype suggests mechanisms of adaptation in cystic fibrosis. Nat. Commun. 12, 3186 (2021). This is a study on the in vivo evolution of P. aeruginosa causing chronic infections in patients with cystic fibrosis who are heavily treated with antibiotics.
pmcid: 8160344
pubmed: 34045458
Luria, S. E. & Delbruck, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28, 491–511 (1943).
pmcid: 1209226
pubmed: 17247100
Navas, A. et al. Experimental validation of Haldane’s hypothesis on the role of infection as an evolutionary force for Metazoans. Proc. Natl Acad. Sci. USA 104, 13728–13731 (2007).
pmcid: 1959450
pubmed: 17699615
Hughes, D. & Andersson, D. I. Evolutionary trajectories to antibiotic resistance. Annu. Rev. Microbiol. 71, 579–596 (2017).
pubmed: 28697667
Gould, S. J. & Vrba, S. Exaptation: a missing term in the science of form. Paleobiology 8, 4–15 (1982).