Informacja

Drogi użytkowniku, aplikacja do prawidłowego działania wymaga obsługi JavaScript. Proszę włącz obsługę JavaScript w Twojej przeglądarce.

Tytuł pozycji:

Compensatory evolution of Pseudomonas aeruginosa's slow growth phenotype suggests mechanisms of adaptation in cystic fibrosis.

Tytuł:
Compensatory evolution of Pseudomonas aeruginosa's slow growth phenotype suggests mechanisms of adaptation in cystic fibrosis.
Autorzy:
La Rosa R; The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark. .
Rossi E; Department of Clinical Microbiology 9301, Rigshospitalet, Copenhagen, Denmark.; Department of Biosciences, Università degli Studi di Milano, Milan, Italy.
Feist AM; The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark.; Department of Bioengineering, University of California, San Diego, CA, USA.
Johansen HK; The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark.; Department of Clinical Microbiology 9301, Rigshospitalet, Copenhagen, Denmark.; Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
Molin S; The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark.
Źródło:
Nature communications [Nat Commun] 2021 May 27; Vol. 12 (1), pp. 3186. Date of Electronic Publication: 2021 May 27.
Typ publikacji:
Journal Article; Research Support, Non-U.S. Gov't
Język:
English
Imprint Name(s):
Original Publication: [London] : Nature Pub. Group
MeSH Terms:
Evolution, Molecular*
Anti-Bacterial Agents/*pharmacology
Cystic Fibrosis/*complications
Drug Resistance, Microbial/*genetics
Pseudomonas Infections/*drug therapy
Pseudomonas aeruginosa/*genetics
Adaptation, Physiological/drug effects ; Adaptation, Physiological/genetics ; Anti-Bacterial Agents/therapeutic use ; Bacterial Proteins/genetics ; Cell Proliferation/drug effects ; Cell Proliferation/genetics ; Cystic Fibrosis/drug therapy ; Cystic Fibrosis/immunology ; Cystic Fibrosis/microbiology ; DNA Mutational Analysis ; DNA, Bacterial/genetics ; DNA, Bacterial/isolation & purification ; Directed Molecular Evolution ; Drug Resistance, Microbial/drug effects ; Gene Expression Regulation, Bacterial ; Genetic Fitness/drug effects ; Genome, Bacterial ; Humans ; Lung/immunology ; Lung/microbiology ; Microbial Sensitivity Tests ; Mutation ; Phenotype ; Pseudomonas Infections/immunology ; Pseudomonas Infections/microbiology ; Pseudomonas aeruginosa/drug effects ; Pseudomonas aeruginosa/isolation & purification ; Sputum/microbiology
References:
Yang, D., Park, S. Y., Park, Y. S., Eun, H. & Lee, S. Y. Metabolic engineering of Escherichia coli for natural product biosynthesis. Trends Biotechnol. 38, 745–765 (2020). (PMID: 3192434510.1016/j.tibtech.2019.11.007)
Pei, L. & Schmidt, M. Fast-growing engineered microbes: new concerns for gain-of-function research? Front. Genet. 9, 207 (2018). (PMID: 30008734603406510.3389/fgene.2018.00207)
Gallagher, T., Phan, J. & Whiteson, K. Getting our fingers on the pulse of slow-growing bacteria in hard-to-reach places. J. Bacteriol. 200, 1–6 (2018). (PMID: 10.1128/JB.00540-18)
Kopf, S. H. et al. Trace incorporation of heavy water reveals slow and heterogeneous pathogen growth rates in cystic fibrosis sputum. Proc. Natl Acad. Sci. U.S.A 113, E110–E116 (2016). (PMID: 2671574110.1073/pnas.1512057112)
Yang, L. et al. In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J. Bacteriol. 190, 2767–2776 (2008). (PMID: 1815625510.1128/JB.01581-07)
La Rosa, R., Johansen, H. K. & Molin, S. Adapting to the airways: metabolic requirements of Pseudomonas aeruginosa during the infection of cystic fibrosis patients. Metabolites 9, 234 (2019). (PMID: 683525510.3390/metabo9100234)
Rossi, E. et al. Pseudomonas aeruginosa adaptation and evolution in patients with cystic fibrosis. Nat. Rev. Microbiol. 19, 331–342 (2021). (PMID: 3321471810.1038/s41579-020-00477-5)
Bartell, J. A. et al. Evolutionary highways to persistent bacterial infection. Nat. Commun. 10, 629 (2019). (PMID: 30733448636739210.1038/s41467-019-08504-7)
La Rosa, R., Johansen, H. K. & Molin, S. Convergent metabolic specialization through distinct evolutionary paths in Pseudomonas aeruginosa. MBio 9, e00269-18 (2018). (PMID: 29636437589387210.1128/mBio.00269-18)
Eng, R. H., Padberg, F. T., Smith, S. M., Tan, E. N. & Cherubin, C. E. Bactericidal effects of antibiotics on slowly growing and nongrowing bacteria. Antimicrob. Agents Chemother. 35, 1824–1828 (1991). (PMID: 195285224527510.1128/AAC.35.9.1824)
Pontes, M. H. & Groisman, E. A. Slow growth determines nonheritable antibiotic resistance in Salmonella enterica. Sci. Signal. 12, 1–11 (2019). (PMID: 10.1126/scisignal.aax3938)
Muir, M. E., van Heeswyck, R. S. & Wallace, B. J. Effect of growth rate on streptomycin accumulation by Escherichia coli and Bacillus megaterium. J. Gen. Microbiol. 130, 2015–2022 (1984). (PMID: 6432955)
Smirnova, G. V. & Oktyabrsky, O. N. Relationship between Escherichia coli growth rate and bacterial susceptibility to ciprofloxacin. FEMS Microbiol. Lett. 365, 1–6 (2018). (PMID: 10.1093/femsle/fnx254)
Marvig, R. L., Sommer, L. M., Molin, S. & Johansen, H. K. Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat. Genet. 47, 57–64 (2015). (PMID: 2540129910.1038/ng.3148)
Hornischer, K. et al. BACTOME—a reference database to explore the sequence- and gene expression-variation landscape of Pseudomonas aeruginosa clinical isolates. Nucleic Acids Res. 47, D716–D720 (2019). (PMID: 3027219310.1093/nar/gky895)
Dettman, J. R. & Kassen, R. Evolutionary genomics of niche-specific adaptation to the cystic fibrosis lung in Pseudomonas aeruginosa. Mol. Biol. Evol. 38, 663–675 (2021). (PMID: 3289827010.1093/molbev/msaa226)
Klockgether, J., Cramer, N., Fischer, S., Wiehlmann, L. & Tümmler, B. Long-term microevolution of Pseudomonas aeruginosa differs between mildly and severely affected cystic fibrosis lungs. Am. J. Respir. Cell Mol. Biol. 59, 246–256 (2018). (PMID: 2947092010.1165/rcmb.2017-0356OC)
Mao, E. F., Lane, L., Lee, J. & Miller, J. H. Proliferation of mutators in A cell population. J. Bacteriol. 179, 417–422 (1997). (PMID: 899029317871110.1128/jb.179.2.417-422.1997)
Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700–702 (1997). (PMID: 919289310.1038/42696)
Tanaka, M. M., Bergstrom, C. T. & Levin, B. R. The evolution of mutator genes in bacterial populations: the roles of environmental change and timing. Genetics 164, 843–854 (2003). (PMID: 12871898146262410.1093/genetics/164.3.843)
Oliver, A. & Mena, A. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin. Microbiol. Infect. 16, 798–808 (2010). (PMID: 2088040910.1111/j.1469-0691.2010.03250.x)
Oliver, A. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288, 1251–1253 (2000). (PMID: 1081800210.1126/science.288.5469.1251)
Feliziani, S. et al. Coexistence and within-host evolution of diversified lineages of hypermutable Pseudomonas aeruginosa in long-term cystic fibrosis infections. PLoS Genet. 10, e1004651 (2014). (PMID: 25330091419949210.1371/journal.pgen.1004651)
Rees, V. E. et al. Characterization of hypermutator Pseudomonas aeruginosa isolates from patients with cystic fibrosis in Australia. Antimicrob. Agents Chemother. 63, 1–11 (2019). (PMID: 10.1128/AAC.02538-18)
Marvig, R. L., Johansen, H. K., Molin, S. & Jelsbak, L. Genome analysis of a transmissible lineage of Pseudomonas aeruginosa reveals pathoadaptive mutations and distinct evolutionary paths of hypermutators. PLoS Genet. 9, e1003741 (2013). (PMID: 24039595376420110.1371/journal.pgen.1003741)
Ciofu, O., Riis, B., Pressler, T., Poulsen, H. E. & Høiby, N. Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob. Agents Chemother. 49, 2276–2282 (2005). (PMID: 15917521114049210.1128/AAC.49.6.2276-2282.2005)
Mena, A. et al. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J. Bacteriol. 190, 7910–7917 (2008). (PMID: 18849421259321410.1128/JB.01147-08)
López-Causapé, C. et al. Evolution of the Pseudomonas aeruginosa mutational resistome in an international cystic fibrosis clone. Sci. Rep. 7, 1–15 (2017). (PMID: 10.1038/s41598-017-05621-5)
Tenaillon, O. et al. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536, 165–170 (2016). (PMID: 27479321498887810.1038/nature18959)
Schick, A. & Kassen, R. Rapid diversification of Pseudomonas aeruginosa in cystic fibrosis lung-like conditions. Proc. Natl Acad. Sci. U.S.A. 115, 10714–10719 (2018). (PMID: 30275334619650710.1073/pnas.1721270115)
Markussen, T. et al. Environmental heterogeneity drives within-host diversification and evolution of Pseudomonas aeruginosa. MBio 5, e01592–14 (2014). (PMID: 25227464417207210.1128/mBio.01592-14)
Passagem-Santos, D., Zacarias, S. & Perfeito, L. Power law fitness landscapes and their ability to predict fitness. Heredity 121, 482–498 (2018). (PMID: 30190560618003810.1038/s41437-018-0143-5)
Lenski, R. E. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J. 11, 2181–2194 (2017). (PMID: 28509909560736010.1038/ismej.2017.69)
Wiser, M. J., Ribeck, N. & Lenski, R. E. Long-term dynamics of adaptation in asexual populations. Science 342, 1364–1367 (2013). (PMID: 2423180810.1126/science.1243357)
Rossi, E., Falcone, M., Molin, S. & Johansen, H. K. High-resolution in situ transcriptomics of Pseudomonas aeruginosa unveils genotype independent patho-phenotypes in cystic fibrosis lungs. Nat. Commun. 9, 3459 (2018). (PMID: 30150613611083110.1038/s41467-018-05944-5)
Cornforth, D. M. et al. Pseudomonas aeruginosa transcriptome during human infection. Proc. Natl Acad. Sci. U.S.A. 115, E5125–E5134 (2018). (PMID: 29760087598449410.1073/pnas.1717525115)
Cornforth, D. M., Diggle, F. L., Melvin, J. A., Bomberger, J. M. & Whiteley, M. Quantitative framework for model evaluation in microbiology research Using Pseudomonas aeruginosa and cystic fibrosis infection as a test case. MBio 11, 1–16 (2020). (PMID: 10.1128/mBio.03042-19)
Webber, M. A. et al. Clinically relevant mutant DNA gyrase alters supercoiling, changes the transcriptome, and confers multidrug resistance. MBio 4, 1–10 (2013). (PMID: 10.1128/mBio.00273-13)
Raji, A., Zabel, D. J., Laufer, C. S. & Depew, R. E. Genetic analysis of mutations that compensate for loss of Escherichia coli DNA topoisomerase I. J. Bacteriol. 162, 1173–1179 (1985). (PMID: 298718421590010.1128/jb.162.3.1173-1179.1985)
Halfon, Y. et al. Structure of Pseudomonas aeruginosa ribosomes from an aminoglycoside-resistant clinical isolate. Proc. Natl Acad. Sci. U.S.A. 116, 22275–22281 (2019). (PMID: 31611393682525510.1073/pnas.1909831116)
Yoon, S. S. et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3, 593–603 (2002). (PMID: 1240881010.1016/S1534-5807(02)00295-2)
Vakulskas, C. A., Potts, A. H., Babitzke, P., Ahmer, B. M. M. & Romeo, T. Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol. Mol. Biol. Rev. 79, 193–224 (2015). (PMID: 25833324439487910.1128/MMBR.00052-14)
Dunai, A. et al. Rapid decline of bacterial drug-resistance in an antibiotic-free environment through phenotypic reversion. Elife 8, 1–20 (2019). (PMID: 10.7554/eLife.47088)
Cookson, W. O. C. M., Cox, M. J. & Moffatt, M. F. New opportunities for managing acute and chronic lung infections. Nat. Rev. Microbiol. 16, 111–120 (2018). (PMID: 2906207010.1038/nrmicro.2017.122)
Rohmer, L., Hocquet, D. & Miller, S. I. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 19, 341–348 (2011). (PMID: 21600774313011010.1016/j.tim.2011.04.003)
Winstanley, C., O’Brien, S. & Brockhurst, M. A. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 24, 327–337 (2016). (PMID: 26946977485417210.1016/j.tim.2016.01.008)
Moradali, M. F., Ghods, S. & Rehm, B. H. A. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front. Cell. Infect. Microbiol. 7, 39 (2017). (PMID: 28261568531013210.3389/fcimb.2017.00039)
Lopatkin, A. J. et al. Bacterial metabolic state more accurately predicts antibiotic lethality than growth rate. Nat. Microbiol. 4, 2109–2117 (2019). (PMID: 31451773687980310.1038/s41564-019-0536-0)
Frimodt-Møller, J. et al. Mutations causing low level antibiotic resistance ensure bacterial survival in antibiotic-treated hosts. Sci. Rep. 8, 12512 (2018). (PMID: 30131514610403110.1038/s41598-018-30972-y)
Francis, V. I. et al. Multiple communication mechanisms between sensor kinases are crucial for virulence in Pseudomonas aeruginosa. Nat. Commun. 9, 2219 (2018).
Henry, R. L., Mellis, C. M. & Petrovic, L. Mucoid Pseudomonas aeruginosa is a marker of poor survival in cystic fibrosis. Pediatr. Pulmonol. 12, 158–161 (1992). (PMID: 164127210.1002/ppul.1950120306)
Rehman, A., Patrick, W. M. & Lamont, I. L. Mechanisms of ciprofloxacin resistance in Pseudomonas aeruginosa: new approaches to an old problem. J. Med. Microbiol. 68, 1–10 (2019). (PMID: 3060507610.1099/jmm.0.000873)
Köhler, T., Harayama, S., Ramos, J. L. & Timmis, K. N. Involvement of Pseudomonas putida RpoN sigma factor in regulation of various metabolic functions. J. Bacteriol. 171, 4326–4333 (1989). (PMID: 266639621020810.1128/jb.171.8.4326-4333.1989)
Viducic, D., Murakami, K., Amoh, T., Ono, T. & Miyake, Y. RpoN promotes Pseudomonas aeruginosa survival in the presence of tobramycin. Front. Microbiol. 8, 839 (2017). (PMID: 28553272542711010.3389/fmicb.2017.00839)
Yang, L. et al. Evolutionary dynamics of bacteria in a human host environment. Proc. Natl Acad. Sci. U.S.A. 108, 7481–7486 (2011). (PMID: 21518885308858210.1073/pnas.1018249108)
Damkiær, S., Yang, L., Molin, S. & Jelsbak, L. Evolutionary remodeling of global regulatory networks during long-term bacterial adaptation to human hosts. Proc. Natl Acad. Sci. U.S.A. 110, 7766–7771 (2013). (PMID: 23610385365141810.1073/pnas.1221466110)
May, T. B. & Chakrabarty, A. M. Pseudomonas aeruginosa: genes and enzymes of alginate synthesis. Trends Microbiol. 2, 151–157 (1994). (PMID: 805517810.1016/0966-842X(94)90664-5)
Khaledi, A. et al. Predicting antimicrobial resistance in Pseudomonas aeruginosa with machine learning‐enabled molecular diagnostics. EMBO Mol. Med. 12, 1–19 (2020). (PMID: 10.15252/emmm.201910264)
Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor laboratory press, 1989).
LaCroix, R. A., Palsson, B. O. & Feist, A. M. A model for designing adaptive laboratory evolution experiments. Appl. Environ. Microbiol. 83, 1–14 (2017). (PMID: 10.1128/AEM.03115-16)
Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, 1–22 (2017). (PMID: 10.1371/journal.pcbi.1005595)
Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016). (PMID: 2700490410.1093/molbev/msw0548210823)
Huang, H. et al. An integrated genomic regulatory network of virulence-related transcriptional factors in Pseudomonas aeruginosa. Nat. Commun. 10, 1–13 (2019).
Qiu, D., Damron, F. H., Mima, T., Schweizer, H. P. & Yu, H. D. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl. Environ. Microbiol. 74, 7422–7426 (2008). (PMID: 18849445259290410.1128/AEM.01369-08)
Kessler, B., de Lorenzo, V. & Timmis, K. N. A general system to integrate lacZ fusions into the chromosomes of gram-negative eubacteria: regulation of the Pm promoter of the TOL plasmid studied with all controlling elements in monocopy. Mol. Gen. Genet. 233, 293–301 (1992). (PMID: 131849910.1007/BF00587591)
Martínez-García, E., Nikel, P. I., Chavarría, M. & de Lorenzo, V. The metabolic cost of flagellar motion in Pseudomonas putida KT2440. Environ. Microbiol. 16, 291–303 (2014). (PMID: 2414802110.1111/1462-2920.12309)
King, E. O., Ward, M. K. & Raney, D. E. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44, 301–307 (1954). (PMID: 13184240)
Sayers, S. et al. Victors: a web-based knowledge base of virulence factors in human and animal pathogens. Nucleic Acids Res. 47, D693–D700 (2019). (PMID: 3036502610.1093/nar/gky999)
Liu, B., Zheng, D., Jin, Q., Chen, L. & Yang, J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 47, D687–D692 (2019). (PMID: 3039525510.1093/nar/gky1080)
Winsor, G. L. et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res. 44, D646–D653 (2016). (PMID: 2657858210.1093/nar/gkv1227)
Schulz, S. et al. Elucidation of sigma factor-associated networks in Pseudomonas aeruginosa reveals a modular architecture with limited and function-specific crosstalk. PLoS Pathog. 11, 1–21 (2015). (PMID: 10.1371/journal.ppat.1004744)
Substance Nomenclature:
0 (Anti-Bacterial Agents)
0 (Bacterial Proteins)
0 (DNA, Bacterial)
Entry Date(s):
Date Created: 20210528 Date Completed: 20210609 Latest Revision: 20230202
Update Code:
20240105
PubMed Central ID:
PMC8160344
DOI:
10.1038/s41467-021-23451-y
PMID:
34045458
Czasopismo naukowe
Long-term infection of the airways of cystic fibrosis patients with Pseudomonas aeruginosa is often accompanied by a reduction in bacterial growth rate. This reduction has been hypothesised to increase within-patient fitness and overall persistence of the pathogen. Here, we apply adaptive laboratory evolution to revert the slow growth phenotype of P. aeruginosa clinical strains back to a high growth rate. We identify several evolutionary trajectories and mechanisms leading to fast growth caused by transcriptional and mutational changes, which depend on the stage of adaptation of the strain. Return to high growth rate increases antibiotic susceptibility, which is only partially dependent on reversion of mutations or changes in the transcriptional profile of genes known to be linked to antibiotic resistance. We propose that similar mechanisms and evolutionary trajectories, in reverse direction, may be involved in pathogen adaptation and the establishment of chronic infections in the antibiotic-treated airways of cystic fibrosis patients.

Ta witryna wykorzystuje pliki cookies do przechowywania informacji na Twoim komputerze. Pliki cookies stosujemy w celu świadczenia usług na najwyższym poziomie, w tym w sposób dostosowany do indywidualnych potrzeb. Korzystanie z witryny bez zmiany ustawień dotyczących cookies oznacza, że będą one zamieszczane w Twoim komputerze. W każdym momencie możesz dokonać zmiany ustawień dotyczących cookies