New insight into bacterial social communication in natural host: Evidence for interplay of heterogeneous and unison quorum response
Autoři:
Biswajit Samal aff001; Subhadeep Chatterjee aff001
Působiště autorů:
Lab of Plant-Microbe Interactions, Centre for DNA Fingerprinting and Diagnostics, Hyderabad, Telengana, India
aff001; Graduate studies, Manipal Academy of Higher Education, Manipal, Karnataka, India
aff002
Vyšlo v časopise:
New insight into bacterial social communication in natural host: Evidence for interplay of heterogeneous and unison quorum response. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008395
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008395
Souhrn
Many microbes exhibit quorum sensing (QS) to cooperate, share and perform a social task in unison. Recent studies have shown the emergence of reversible phenotypic heterogeneity in the QS-responding pathogenic microbial population under laboratory conditions as a possible bet-hedging survival strategy. However, very little is known about the dynamics of QS-response and the nature of phenotypic heterogeneity in an actual host-pathogen interaction environment. Here, we investigated the dynamics of QS-response of a Gram-negative phytopathogen Xanthomonas pv. campestris (Xcc) inside its natural host cabbage, that communicate through a fatty acid signal molecule called DSF (diffusible signal factor) for coordination of several social traits including virulence functions. In this study, we engineered a novel DSF responsive whole-cell QS dual-bioreporter to measure the DSF mediated QS-response in Xcc at the single cell level inside its natural host plant in vivo. Employing the dual-bioreporter strain of Xcc, we show that QS non-responsive cells coexist with responsive cells in microcolonies at the early stage of the disease; whereas in the late stages, the QS-response is more homogeneous as the QS non-responders exhibit reduced fitness and are out competed by the wild-type. Furthermore, using the wild-type Xcc and its QS mutants in single and mixed infection studies, we show that QS mutants get benefit to some extend at the early stage of disease and contribute to localized colonization. However, the QS-responding cells contribute to spread along xylem vessel. These results contrast with the earlier studies describing that expected cross-induction and cooperative sharing at high cell density in vivo may lead to synchronize QS-response. Our findings suggest that the transition from heterogeneity to homogeneity in QS-response within a bacterial population contributes to its overall virulence efficiency to cause disease in the host plant under natural environment.
Klíčová slova:
Biology and life sciences – Plant science – Plant anatomy – Leaves – Plant cell biology – Mesophyll – Plant pathology – Plant pathogens – Plant bacterial pathogens – Organisms – Eukaryota – Plants – Brassica – Cell biology – Research and analysis methods – Microscopy – Light microscopy – Confocal microscopy – Confocal laser microscopy – Imaging techniques – Fluorescence imaging
Zdroje
1. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology. 1994; 176(2): 269–275. doi: 10.1128/jb.176.2.269-275.1994 8288518
2. Von Bodman SB, Bauer WD, Coplin DL. Quorum sensing in plant-pathogenic bacteria. Annual Review of Phytopathology. 2003; 41(1): 455–482.
3. Waters CM, Bassler BL. Quorum sensing: Cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology. 2005; 21(1): 319–346.
4. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annual Review of Genetics. 2009; 43: 197–222. doi: 10.1146/annurev-genet-102108-134304 19686078
5. Darch SE, West SA, Winzer K, Diggle SP. Density-dependent fitness benefits in quorum-sensing bacterial populations. Proceedings of the National Academy of Sciences. 2012; 109(21): 8259–8263.
6. Pai A, Tanouchi Y, You L. Optimally and robustness in quorum sensing (QS) mediated regulation of a costly public good enzyme. Proceedings of the National Academy of Sciences. 2012; 109(48): 19810–19815.
7. West SA, Winzer K, Gardner A, Diggle SP. Quorum sensing and the confusion about diffusion. Trends in Microbiology. 2012; 20(12): 586–594. doi: 10.1016/j.tim.2012.09.004 23084573
8. Anetzberger C, Pirch T, Jung K. Heterogeneity in quorum sensing regulated bioluminescence of Vibrio harveyi. Molecular Microbiology. 2009; 73(2): 267–277. doi: 10.1111/j.1365-2958.2009.06768.x 19555459
9. Pradhan BB, Chatterjee S. Reversible non-genetic phenotypic heterogeneity in bacterial quorum sensing. Molecular Microbiology. 2014; 92(3): 557–569. doi: 10.1111/mmi.12575 24601980
10. Ca´rcamo-Oyarce G, Lumjiaktase P, Ku¨mmerli R, Eberl L. Quorum sensing triggers the stochastic escape of individual cells from Pseudomonas putida biofilms. Nature Communications. 2015; 6: 5945. doi: 10.1038/ncomms6945 25592773
11. Bauer M, Knebel J, Lechner M, Pickl P, Frey E. Ecological feedback in quorum-sensing microbial populations can induce heterogeneous production of autoinducers. eLife. 2017; 6: e25773. doi: 10.7554/eLife.25773 28741470
12. Kaplan HB, Greenberg EP. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. Journal of Bacteriology. 1985; 163(3): 1210–1214. 3897188
13. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology. 2012; 13(6): 614–629. doi: 10.1111/j.1364-3703.2012.00804.x 22672649
14. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, et al. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Molecular Microbiology. 1997; 24(3): 555–566. doi: 10.1046/j.1365-2958.1997.3721736.x 9179849
15. Rai R, Pradhan BB, Ranjan M, Chatterjee S. Atypical regulation of virulence associated functions by a Diffusible Signal Factor in Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions. 2012; 25(6): 789–801. doi: 10.1094/MPMI-11-11-0285-R 22352717
16. Deng Y, Wu JE, Tao F, Zhang LH. Listening to a new language: DSF-based quorum sensing in negative-Gram bacteria. Chem. Rev. 2011; 111(1): 160–173. doi: 10.1021/cr100354f 21166386
17. Ryan RP, An SQ, Allan JH, McCarthy Y, Dow JM. The DSF-family of cell-cell signals: An expanding class of bacterial virulence regulators. PLoS Pathogens. 2015; 11(7): e1004986. doi: 10.1371/journal.ppat.1004986 26181439
18. Dandekar AA, Chugani S, Greenberg EP. Bacterial quorum sensing and metabolic incentives to cooperate. Science. 2012; 338(6104), 264–266. doi: 10.1126/science.1227289 23066081
19. Zhou L, Slamti L, Nielsen-LeRoux C, Lereclus D, Raymond B. The Social Biology of Quorum Sensing in a Naturalistic Host Pathogen System. Current Biology. 2014; 24(20): 2417–2422. doi: 10.1016/j.cub.2014.08.049 25308072
20. Schuster M, Sexton DJ, Hense BA. Why Quorum Sensing Controls Private Goods. Frontiers in Microbiology. 2017; 8: 885. doi: 10.3389/fmicb.2017.00885 28579979
21. Cook AA, Walker JC, Larson RH. Studies on the disease cycle of black rot of crucifers. Phytopathology. 1952; 42: 162–167.
22. Parker JE, Barber CE, Fan MJ, Daniels MJ. Interaction of Xanthomonas campestris with Arabidopsis thaliana: Characterization of a gene from Xanthomonas campestris pv. raphani that confers avirulence to most A. thaliana accessions. Molecular Plant-Microbe Interactions. 1993; 6(2): 216–224. 8471795
23. Akimoto-Tomiyama C, Furutani A, Ochiai H. Real Time Live Imaging of Phytopathogenic Bacteria Xanthomonas campestris pv. campestris MAFF106712 in ‘Plant Sweet Home’. PLoS ONE. 2014; 9(4): e94386. doi: 10.1371/journal.pone.0094386 24736478
24. Mensi I, Vernerey M, Gargani D, Nicole M, Rott P. Breaking dogmas: the plant vascular pathogen Xanthomonas albilineans is able to invade non-vascular tissues despite its reduced genome. Open Biology. 2016; 4(2): e130116.
25. Harrison F, Browning LE, Vos M, Buckling A. Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biology. 2006; 4: 21. doi: 10.1186/1741-7007-4-21 16827933
26. Raymond B, West SA, Griffin AS, Bonsall MB. The dynamics of cooperative bacterial virulence in the field. Science. 2012; 337(6090): 85–88. doi: 10.1126/science.1218196 22767928
27. Slamti L, Perchat S, Gominet M, Vilas-Boˆ as G, Fouet A, Mock M, et al. Distinct mutations in PlcR explain why some strains of the Bacillus cereus group are non-hemolytic. Journal of Bacteriology. 2004; 186(11), 3531–3538. doi: 10.1128/JB.186.11.3531-3538.2004 15150241
28. Torres PS, Malamud F, Rigano LA, Russo DM, Marano MR, Castagnaro AP, et al. Controlled synthesis of the DSF cell–cell signal is required for biofilm formation and virulence in Xanthomonas campestris. Environmental Microbiology. 2007; 9(8): 2101–2109. doi: 10.1111/j.1462-2920.2007.01332.x 17635553
29. Newman KL, Almeida RPP, Purcell AH, and Lindow SE. Cell–cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proceedings of the National Academy of Sciences. 2004; 101 (6): 1737–1742.
30. Khokhani D, Lowe-Power TM, Tran TM, Allen C. A Single Regulator Mediates Strategic Switching between Attachment/Spread and Growth/Virulence in the Plant Pathogen Ralstonia solanacearum. mBio. 2017; 8 (5): e00895–17. doi: 10.1128/mBio.00895-17 28951474
31. Pandey SS, Patnana PK, Lomada SK, Tomar A, Chatterjee S. Co-regulation of Iron Metabolism and Virulence Associated Functions by Iron and XibR, a Novel Iron Binding ranscription Factor, in the Plant Pathogen Xanthomonas. PLoS Pathogens. 2016; 12(11): e1006019. doi: 10.1371/journal.ppat.1006019 27902780
32. Demoling F, Figueroa D, Baath E. Comparison of factors limiting bacterial growth in different soils. Soil Biology & Biochemistry. 2007; 39(10): 2485–2495.
33. Diard M, Garcia V, Maier L, Remus-Emsermann MN, Regoes RR, Ackermann M, Hardt WD. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature. 2013; 494(7437): 353–356. doi: 10.1038/nature11913 23426324
34. Rajeshwari R, Sonti RV. Stationary-phase variation due to transposition of novel insertion elements in Xanthomonas oryzae pv. oryzae. Journal of Bacteriology. 2000; 182(17): 4797–4802. doi: 10.1128/jb.182.17.4797-4802.2000 10940020
35. Miller JH. A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia Coli and Related Bacteria. 1992; Vol. 1. CSHL Press, Cold Spring Harbor, NY, USA.
36. Tsuchia K, Mew TW, Wakimoto S. Bacteriological and pathological charecteristics of wild-types and induced mutants of Xanthomonas campestris pv. oryzae. Phytopathology. 1982; 72(1): 43–46.
37. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM II, et al. Four new derivatives of the broad-host-range cloning vector pBBR1 MCS, carrying different antibiotic-resistance cassettes. Gene. 1995; 166(1): 175–176. doi: 10.1016/0378-1119(95)00584-1 8529885
38. Bonas U, Stall RE, Staskawicz B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Molecular and General Genetics. 1989; 218(1): 127–136. doi: 10.1007/bf00330575 2550761
39. Jefferson RA, Kavanagh TA, Bevan MW. GUS fusions: B-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal. 1987; 6(13): 3901–3907. 3327686
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 9
Nejčtenější v tomto čísle
- Origins of DNA replication
- Environmental and epigenetic regulation of Rider retrotransposons in tomato
- Integrating transcriptomic network reconstruction and eQTL analyses reveals mechanistic connections between genomic architecture and Brassica rapa development
- Temperature preference can bias parental genome retention during hybrid evolution