Extracellular products-mediated interspecific interaction between Pseudomonas aeruginosa and Escherichia coli

다국어 초록 (Multilingual Abstract)

The Gram-negative pathogen Pseudomonas aeruginosa adopts several elaborate strategies to colonize a wide range of natural or clinical niches and to overcome the neighboring bacterial competitors in polymicrobial communities. However, the relationship and interaction mechanism of P. aeruginosa with other bacterial pathogens remains largely unexplored.
Here we explore the interaction dynamics of P. aeruginosa and Escherichia coli, which frequently coinfect the lungs of immunocompromised hosts, by using a series of on-plate proximity assays and RNA-sequencing. We show that the extracellular products of P. aeruginosa can inhibit the growth of neighboring E. coli and induce a large-scale of transcriptional reprogramming of E. coli, especially in terms of cellular respiration- related primary metabolisms and membrane components.
In contrast, the presence of E. coli has no significant effect on the growth of P. aeruginosa in short-term culture, but causes a dysregulated expression of genes positively controlled by the quorum-sensing (QS) system of P. aeruginosa during subsequent pairwise culture. We further demonstrate that the divergent QS-regulation of P. aeruginosa may be related to the function of the transcriptional regulator PqsR, which can be enhanced by E. coli culture supernatant to increase the pyocyanin production by P. aeruginosa in the absence of the central las-QS system. Moreover, the extracellular products of E. coli promote the proliferation and lethality of P. aeruginosa in infecting the Caenorhabditis elegans model. The current study provides a general characterization of the extracellular products-mediated interactions between P. aeruginosa and E. coli, and may facilitate the understanding of polymicrobial infections.

참고문헌 (Reference)

1 Orazi, G., "‘It takes a village’ : mechanisms underlying antimicrobial recalcitrance of polymicrobial biofilms" 202 : e00530-19, 2019

2 Pragman, A. A., "Understanding persistent bacterial lung infections : clinical implications informed by the biology of the microbiota and biofilms" 23 : 57-66, 2016

3 Tognon, M., "Transcriptional profiling of Pseudomonas aeruginosa and Staphylococcus aureus during in vitro co-culture" 20 : 30-, 2019

4 Nadell, C. D., "The sociobiology of biofilms" 33 : 206-224, 2009

5 Jimenez, P. N., "The multiple signaling systems regulating virulence in Pseudomonas aeruginosa" 76 : 46-65, 2012

6 Toyofuku, M., "The effect of a cell-to-cell communication molecule, Pseudomonas quinolone signal (PQS), produced by P. aeruginosa on other bacterial species" 25 : 1-7, 2010

7 Déziel, E., "The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones" 55 : 998-1014, 2005

8 Stacy, A., "The biogeography of polymicrobial infection" 14 : 93-105, 2016

9 Scott, J. E., "The Yin and Yang of Streptococcus lung infections in cystic fibrosis : a model for studying polymicrobial interactions" 201 : e00115-19, 2019

10 Lin, J., "The Pseudomonas quinolone signal(PQS) : not just for quorum sensing anymore" 8 : 230-, 2018

11 Diggle, S. P., "The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR" 50 : 29-43, 2003

12 Diggle, S. P., "The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment" 14 : 87-96, 2007

13 Zhao, K., "TesG is a type I secretion effector of Pseudomonas aeruginosa that suppresses the host immune response during chronic infection" 4 : 459-469, 2019

14 Huang, D. W., "Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources" 4 : 44-57, 2009

15 Joao B. Xavier, "Sociomicrobiology and Pathogenic Bacteria" American Society for Microbiology 4 (4): 2016

16 Sandoz, K. M., "Social cheating in Pseudomonas aeruginosa quorum sensing" 104 : 15876-15881, 2007

17 Little, A. E., "Rules of engagement : interspecies interactions that regulate microbial communities" 62 : 375-401, 2008

18 Tashiro, Y., "Pseudomonas quinolone signal affects membrane vesicle production in not only Gram-negative but also Grampositive bacteria" 25 : 120-125, 2010

19 Zhao, K., "Pseudomonas aeruginosa quorumsensing and type VI secretion system can direct interspecific coexistence during evolution" 9 : 2287-, 2018

20 Rodrigo-Troyano, A., "Pseudomonas aeruginosa in chronic obstructive pulmonary disease patients with frequent hospitalized exacerbations : a prospective multicentre study" 96 : 417-424, 2018

21 Korgaonkar, A. K., "Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan" 193 : 909-917, 2011

22 Zhao, K., "Population divergence of Pseudomonas aeruginosa can lead to the coexistence with Escherichia coli in animal suppurative lesions" 231 : 169-176, 2019

23 Peters, B. M., "Polymicrobial interactions : impact on pathogenesis and human disease" 25 : 193-213, 2012

24 Short, F. L., "Polybacterial human disease : the ills of social networking" 22 : 508-516, 2014

25 Zhao, K., "Phenotypic and genetic characterization of Pseudomonas aeruginosa isolate COP2 from the lung of COPD patients in China" 77 : ftz038-, 2019

26 Magill, S. S., "Multistate point-prevalence survey of health care-associated infections" 370 : 1198-1208, 2014

27 Khare, A., "Multifactorial competition and resistance in a two-species bacterial system" 11 : e1005715-, 2015

28 Elias, S., "Multi-species biofilms : living with friendly neighbors" 36 : 990-1004, 2012

29 Baron, S. S., "Molecular mechanism of the antimicrobial action of pyocyanin" 18 : 223-230, 1989

30 Tan, M. W., "Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis" 96 : 715-720, 1999

31 Tashiro, Y., "Interspecies interaction between Pseudomonas aeruginosa and other microorganisms" 28 : 13-24, 2013

32 Solden, L. M., "Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem" 3 : 1274-1284, 2018

33 Vandeplassche, E., "Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens" 28 : 190041-, 2019

34 Chu, W., "Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling" 78 : 411-419, 2012

35 Hotterbeekx, A., "In vivo and in vitro interactions between Pseudomonas aeruginosa and Staphylococcus spp" 7 : 106-, 2017

36 Schuster, M., "Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis" 185 : 2066-2079, 2003

37 Essar, D. W., "Identi-fication and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa : interchangeability of the two anthranilate synthases and evolutionary implications" 172 : 884-900, 1990

38 Hazan, R., "Homeostatic interplay between bacterial cell-cell signaling and iron in virulence" 6 : e1000810-, 2010

39 최유상, "Growth Phase-Differential Quorum Sensing Regulation of Anthranilate Metabolism in Pseudomonas aeruginosa" 한국분자세포생물학회 32 (32): 57-65, 2011

40 Smith, E. E., "Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients" 103 : 8487-8492, 2006

41 Young, M. D., "Gene ontology analysis for RNA-seq : accounting for selection bias" 11 : R14-, 2010

42 Gallagher, L. A., "Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa" 184 : 6472-6480, 2002

43 Langmead, B., "Fast gapped-read alignment with Bowtie 2" 9 : 357-359, 2012

44 Frydenlund Michelsen, C., "Evolution of metabolic divergence in Pseudomonas aeruginosa during longterm infection facilitates a proto-cooperative interspecies interaction" 10 : 1323-1336, 2016

45 Azimi, T., "Evaluating the antimicrobial resistance patterns among major bacterial pathogens isolated from clinical specimens taken from patients in Mofid Children’s Hospital, Tehran, Iran: 2013-2018" 12 : 2089-2102, 2019

46 Keogh, D., "Enterococcal metabolite cues facilitate interspecies niche modulation and polymicrobial infection" 20 : 493-503, 2016

47 Whiley, R. A., "Differential potentiation of the virulence of the Pseudomonas aeruginosa cystic fibrosis liverpool epidemic strain by oral commensal Streptococci" 209 : 769-780, 2014

48 Trapnell, C., "Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks" 7 : 562-578, 2012

49 Wang, L., "DEGseq : an R package for identifying differentially expressed genes from RNA-seq data" 26 : 136-138, 2010

50 Tshikantwa, T. S., "Current trends and potential applications of microbial interactions for human welfare" 9 : 1156-, 2018

51 Frost, I., "Cooperation, competition and antibiotic resistance in bacterial colonies" 12 : 1582-1593, 2018

52 Köhler, T., "Cooperation and virulence of clinical Pseudomonas aeruginosa populations" 106 : 6339-6344, 2009

53 Strateva, T., "Contribution of an arsenal of virulence factors to pathogenesis of Pseudomonas aeruginosa infections" 61 : 717-732, 2011

54 Jacobs, M. A., "Comprehensive transposon mutant library of Pseudomonas aeruginosa" 100 : 14339-14344, 2003

55 Foster, K. R., "Competition, not cooperation, dominates interactions among culturable microbial species" 22 : 1845-1850, 2012

56 Sommerstein, R., "Characterizing non-linear effects of hospitalisation duration on antimicrobial resistance in respiratory isolates : an analysis of a prospective nationwide surveillance system" 24 : 45-52, 2018

57 Dandekar, A. A., "Bacterial quorum sensing and metabolic incentives to cooperate" 338 : 264-266, 2012

58 Cao, H., "A quorum sensing-associated virulence gene of Pseudomonas aeruginosa encodes a LysR-like transcription regulator with a unique self-regulatory mechanism" 98 : 14613-14618, 2001

59 Balasubramanian, D., "A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence" 41 : 1-20, 2013