Molecular and chemical dialogues in bacteria-protozoa interactions

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Song, Chunxu ^a,f   Mazzola, Mark ^b   Cheng, Xu ^a   Oetjen, Janina ^c   Alexandrov, Theodore ^c,d,e   Dorrestein, Pieter ^d   Watrous, Jeramie ^d   Van Der Voort, Menno ^a   Raaijmakers, Jos M ^a,f  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF BREMEN   (Germany)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^f NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPEPTIDE; PUTRESCINE; TRANSCRIPTOME;

GENETICS; METABOLISM; NAEGLERIA; PHYSIOLOGY; PSEUDOMONAS FLUORESCENS;

LIPOPEPTIDES; NAEGLERIA; PSEUDOMONAS FLUORESCENS; PUTRESCINE; TRANSCRIPTOME;

EID: 84938901868     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12837     Document Type: Article

References (58)

1. Bonkowski, M., Villenave, C. & Griffiths, B. Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321, 213-233, doi: 10.1007/s11104-009-0013-2 (2009).
2. Buee, M., De Boer, W., Martin, F., van Overbeek, L. & Jurkevitch, E. The rhizosphere zoo: An overview of plant-Associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321, 189-212, doi: 10.1007/s11104-009-9991-3 (2009).
3. Mendes, R., Garbeva, P. & Raaijmakers, J. M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. Fems Microbiol Rev 37, 634-663, doi: 10.1111/1574-6976.12028 (2013).
4. Philippot, L., Raaijmakers, J. M., Lemanceau, P. & van der Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nature reviews. Microbiology 11, 789-799, doi: 10.1038/nrmicro3109 (2013).
5. Taylor, W. D. Growth responses of ciliate protozoa to abundance of their bacterial prey. Microbial Ecol 4, 207-214 (1978).
6. Ronn, R., McCaig, A. E., Griffiths, B. S. & Prosser, J. I. Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microb 68, 6094-6105, doi: 10.1128/Aem.68.12.6094-6105.2002 (2002).
7. Bonkowski, M. & Brandt, F. Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34, 1709-1715, doi: 10.1016/S0038-0717(02)00157-8 (2002).
8. Cohen, M. F. & Mazzola, M. Effects of Brassica napus seed meal amendment on soil populations of resident bacteria and Naegleria americana, and the unsuitability of arachidonic acid as a protozoan-specific marker. Journal of Protozoology Research 16, 16-25 (2006).
9. Alexandrov, T. et al. Spatial segmentation of imaging mass spectrometry data with edge-preserving image denoising and clustering. J Proteome Res 9, 6535-6546, doi: 10.1021/Pr100734z (2010).
10. Matz, C. & Kjelleberg, S. Off the hook-how bacteria survive protozoan grazing. Trends Microbiol 13, 302-307, doi: 10.1016/j. tim.2005.05.009 (2005).
11. Brown, M. R. W. & Barker, J. Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol 7, 46-50, doi: 10.1016/S0966-842x(98)01425-5 (1999).
12. Hahn, M. W. & Hofle, M. G. Grazing pressure by a bacterivorous flagellate reverses the relative abundance of Comamonas acidovorans PX54 and Vibrio strain CB5 in chemostat cocultures. Appl Environ Microb 64, 1910-1918 (1998).
13. Hahn, M. W., Moore, E. R. B. & Hofle, M. G. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl Environ Microb 65, 25-35 (1999).
14. Pernthaler, J., Zollner, E., Warnecke, F. & Jurgens, K. Bloom of filamentous bacteria in a mesotrophic lake: identity and potential controlling mechanism. Appl Environ Microb 70, 6272-6281, doi: 10.1128/Aem.70.10.6272-6281.2004 (2004).
15. Matz, C. & Jurgens, K. High motility reduces grazing mortality of planktonic bacteria. Appl Environ Microb 71, 921-929, doi: 10.1128/Aem.71.2.921-929.2005 (2005).
16. Matz, C., Bergfeld, T., Rice, S. A. & Kjelleberg, S. Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6, 218-226, doi: 10.1111/j.1462-2920.2004. 00556.x (2004).
17. Cosson, P. et al. Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184, 3027-3033, doi: 10.1128/Jb.184.11.3027-3033.2002 (2002).
18. Pukatzki, S., Kessin, R. H. & Mekalanos, J. J. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. P Natl Acad Sci USA 99, 3159-3164, doi: 10.1073/pnas.052704399 (2002).
19. Jousset, A., Rochat, L., Scheu, S., Bonkowski, M. & Keel, C. Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere-Associated Pseudomonas fluorescens. Appl Environ Microb 76, 5263-5268, doi: 10.1128/Aem.02941-09 (2010).
20. Gallagher, L. A. & Manoil, C. Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183, 6207-6214, doi: 10.1128/Jb.183.21.6207-6214.2001 (2001).
21. Jousset, A., Lara, E., Wall, L. G. & Valverde, C. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microb 72, 7083-7090, doi: 10.1128/Aem.00557-06 (2006).
22. Vaitkevicius, K. et al. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. P Natl Acad Sci USA 103, 9280-9285, doi: 10.1073/pnas.0601754103 (2006).
23. Niu, Q. H. et al. A Trojan horse mechanism of bacterial pathogenesis against nematodes. P Natl Acad Sci USA 107, 16631-16636, doi: 10.1073/pnas.1007276107 (2010).
24. Mazzola, M., de Bruijn, I., Cohen, M. F. & Raaijmakers, J. M. Protozoan-induced regulation of cyclic lipopeptide biosynthesis is an effective predation defense mechanism for Pseudomonas fluorescens. Appl Environ Microb 75, 6804-6811, doi: 10.1128/Aem.01272-09 (2009).
25. Yang, Y. L., Xu, Y., Straight, P. & Dorrestein, P. C. Translating metabolic exchange with imaging mass spectrometry. Nature chemical biology 5, 885-887, doi: 10.1038/nchembio.252 (2009).
26. Watrous, J. D. & Dorrestein, P. C. Imaging mass spectrometry in microbiology. Nature reviews. Microbiology 9, 683-694, doi: 10.1038/nrmicro2634 (2011).
27. Esquenazi, E., Yang, Y. L., Watrous, J., Gerwick, W. H. & Dorrestein, P. C. Imaging mass spectrometry of natural products. Natural product reports 26, 1521-1534, doi: 10.1039/b915674g (2009).
28. Lorca, G., Winnen, B. & Saier, M. H., Jr. Identification of the L-Aspartate transporter in Bacillus subtilis. J Bacteriol 185, 3218-3222 (2003).
29. Mitra, A. & Sarma, S. P. Escherichia coli ilvN interacts with the FAD binding domain of ilvB and activates the AHAS I enzyme. Biochemistry 47, 1518-1531, doi: 10.1021/bi701893b (2008).
30. Nelson, D. R. & Duxbury, T. The distribution of acetohydroxyacid synthase in soil bacteria. Anton Leeuw Int J G 93, 123-132, doi: 10.1007/s10482-007-9186-y (2008).
31. de Bruijn, I. & Raaijmakers, J. M. Regulation of cyclic lipopeptide biosynthesis in Pseudomonas fluorescens by the ClpP protease. J Bacteriol 191, 1910-1923, doi: 10.1128/Jb.01558-08 (2009).
32. Strauss, S. L., Kidarsa, T., Loper, J. & Mazzola, M. Secondary metabolite production by Pseudomonas fluorescens strain Pf-5 confers protection against Naegleria americana in the wheat rhizosphere (2011).
33. Ramos, J. L. et al. The TetR family of transcriptional repressors. Microbiology and molecular biology reviews : MMBR 69, 326-356, doi: 10.1128/MMBR.69.2.326-356.2005 (2005).
34. Cuthbertson, L. & Nodwell, J. R. The TetR family of regulators. Microbiology and molecular biology reviews : MMBR 77, 440-475, doi: 10.1128/MMBR.00018-13 (2013).
35. Guo, J. et al. A novel TetR family transcriptional regulator, SAV576, negatively controls avermectin biosynthesis in Streptomyces avermitilis. PloS one 8, e71330, doi: 10.1371/journal.pone.0071330 (2013).
36. Hardegger, M., Koch, A. K., Ochsner, U. A., Fiechter, A. & Reiser, J. Cloning and heterologous expression of a gene encoding an alkane-induced extracellular protein involved in alkane assimilation from Pseudomonas aeruginosa. Appl Environ Microbiol 60, 3679-3687 (1994).
37. Fiechter, A. Biosurfactants-moving towards industrial application. Trends Biotechnol 10, 208-217, doi: 10.1016/0167-7799(92) 90215-H (1992).
38. Urs, A. & Ochsner, T. H. Armin Fiechter. Production of rhamnolipid biosurfactants. Advances in Biochemical Engineering/Biotechnology 53, 89-118 (1996).
39. Rojo, F. Degradation of alkanes by bacteria. Environ Microbiol 11, 2477-2490, doi: 10.1111/j.1462-2920.2009.01948.x (2009).
40. Fenton, A. M., Stephens, P. M., Crowley, J., O'Callaghan, M. & O'Gara, F. Exploitation of gene(s) involved in 2,4-diacetylphlor oglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Appl Environ Microbiol 58, 3873-3878 (1992).
41. Keel, C. et al. Suppression of root diseases by Pseudomonas fluorescens Cha0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant Microbe In 5, 4-13, doi: 10.1094/Mpmi-5-004 (1992).
42. Nakada, Y. & Itoh, Y. Identification of the putrescine biosynthetic genes in Pseudomonas aeruginosa and characterization of agmatine deiminase and N-carbamoylputrescine amidohydrolase of the arginine decarboxylase pathway. Microbiology 149, 707-714 (2003).
43. Cunin, R., Glansdorff, N., Pierard, A. & Stalon, V. Biosynthesis and metabolism of arginine in bacteria. Microbiological reviews 50, 314-352 (1986).
44. Tabor, C. W. & Tabor, H. Polyamines in microorganisms. Microbiological reviews 49, 81-99 (1985).
45. Kuiper, I., Bloemberg, G. V., Noreen, S., Thomas-Oates, J. E. & Lugtenberg, B. J. J. Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe In 14, 1096-1104, doi: 10.1094/Mpmi.2001.14.9.1096 (2001).
46. Sturgill, G. & Rather, P. N. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol Microbiol 51, 437-446, doi: 10.1046/j.1365-2958.2003.03835.x (2004).
47. Chattopadhyay, M. K., Tabor, C. W. & Tabor, H. Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci U S A 100, 2261-2265, doi: 10.1073/pnas.2627990100 (2003).
48. Wortham, B. W., Oliveira, M. A., Fetherston, J. D. & Perry, R. D. Polyamines are required for the expression of key Hms proteins important for Yersinia pestis biofilm formation. Environ Microbiol 12, 2034-2047, doi: 10.1111/j.1462-2920.2010.02219.x (2010).
49. Watrous, J. et al. Mass spectral molecular networking of living microbial colonies. P Natl Acad Sci USA 109, E1743-E1752, doi: 10.1073/pnas.1203689109 (2012).
50. de Bruijn, I., de Kock, M. J. D., de Waard, P., van Beek, T. A. & Raaijmakers, J. M. Massetolide A biosynthesis in Pseudomonas fluorescens. J Bacteriol 190, 2777-2789, doi: 10.1128/Jb.01563-07 (2008).
51. Moree, W. J. et al. Imaging mass spectrometry of a coral microbe interaction with fungi. J Chem Ecol 39, 1045-1054, doi: 10.1007/s10886-013-0320-1 (2013).
52. Traxler, M. F., Watrous, J. D., Alexandrov, T., Dorrestein, P. C. & Kolter, R. Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. Mbio 4, doi: ARTN e00459-13. DOI 10.1128/mBio.00459-13 (2013).
53. Moree, W. J. et al. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. P Natl Acad Sci USA 109, 13811-13816, doi: 10.1073/pnas.1206855109 (2012).
54. Rowbotham, T. J. Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J Clin Pathol 36, 978-986, doi: 10.1136/Jcp.36.9.978 (1983).
55. de Knegt, G. J. et al. Rifampicin-induced transcriptome response in rifampicin-resistant Mycobacterium tuberculosis. Tuberculosis 93, 96-101, doi: 10.1016/j.tube.2012.10.013 (2013).
56. Pennings, J. L. et al. Gene expression profiling in a mouse model identifies fetal liver-And placenta-derived potential biomarkers for down syndrome screening. PloS one 6, e18866, doi: 10.1371/journal.pone.0018866 (2011).
57. Alexandrov, T., Becker, M., Guntinas-Lichius, O., Ernst, G. & von Eggeling, F. MALDI-imaging segmentation is a powerful tool for spatial functional proteomic analysis of human larynx carcinoma. J Cancer Res Clin 139, 85-95, doi: 10.1007/s00432-012-1303-2 (2013).
58. Trede, D. et al. Exploring three-dimensional matrix-Assisted laser desorption/ionization imaging mass spectrometry data: threedimensional spatial segmentation of mouse kidney. Anal Chem 84, 6079-6087, doi: 10.1021/Ac300673y (2012).