Endophytes-assisted biocontrol: novel insights in ecology and the mode of action of Paenibacillus

Plant and Soil

Volumn 405, Issue 1-2, 2016, Pages 125-140

  Rybakova, Daria ^a   Cernava, Tomislav ^a   Köberl, Martina ^a,b   Liebminger, Stefan ^c   Etemadi, Mohammad ^a,b   Berg, Gabriele ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^c Roombiotic GmbH   (Austria)

Author keywords

Endophyte; Metagenomics; PGPR; Plant growth promotion; Volatiles

Indexed keywords

ALTERNATIVE AGRICULTURE; ANTAGONISM; BACTERIUM; BIOCONTROL AGENT; BIOLOGICAL CONTROL; COLONIZATION; CROP DAMAGE; ENDOPHYTE; LIFESTYLE; PATHOGEN; VOLATILE ORGANIC COMPOUND;

BACTERIA (MICROORGANISMS); PAENIBACILLUS;

EID: 84931846861     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-015-2526-1     Document Type: Article

References (116)

1. Aguilar C, Vlamakis H, Losick R, Kolter R (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10:638–643
2. Alvarez VM, von der Weid I, Seldin L, Santos AL (2006) Influence of growth conditions on the production of extracellular proteolytic enzymes in Paenibacillus peoriae NRRL BD-62 and Paenibacillus polymyxa SCE2. Lett Appl Microbiol 43:625–630
3. Anand R, Paul L, Chanway C (2006) Research on endophytic bacteria: recent advances with forest trees. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin Heidelberg, pp 89–106
4. Antonopoulos DF, Tjamos SE, Antoniou PP, Rafeletos P, Tjamos EC (2008) Effect of Paenibacillus alvei, strain K165, on the germination of Verticillium dahliae microsclerotia in planta. Biol Control 46:166–170
5. Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wllbanks and Collins) using a PCR probe test. Antonie Van Leeuwenhoek 64:253–260
6. Aswathy AJ, Jasim B, Jyothis M, Radhakrishnan EK (2013) Identification of two strains of Paenibacillus sp. as indole 3 acetic acid-producing rhizome-associated endophytic bacteria from Curcuma longa. 3. Biotech 3:219–224
7. Bacon CW, Hinton DM (1997) Isolation and culture of endophytic bacteria and fungi. In: Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. ASM Press, Washington, pp 413–421
8. Beatty PH, Jensen SE (2002) Paenibacillus polymyxa produces fusaricidin-type antifungal antibiotics active against Leptosphaeria maculans, the causative agent of blackleg disease of canola. Can J Microbiol 48:159–169
9. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 23:E1621–E1630
10. Beck HC, Hansen AM, Lauritsen FR (2003) Novel pyrazine metabolites found in polymyxin biosynthesis by Paenibacillus polymyxa. FEMS Microbiol Lett 220:67–73
11. Ben-Jacob E, Becker I, Shapira Y, Levine H (2004) Bacterial linguistic communication and social intelligence. Trends Microbiol 12:366–372
12. Bent E, Chanway CP (1998) The growth-promoting effects of a bacterial endophyte on lodgepole pine are partially inhibited by the presence of other rhizobacteria. Can J Microbiol 44:980–988
13. Bent E, Chanway CP (2002) Potential for misidentification of a spore-forming Paenibacillus polymyxa isolate as an endophyte by using culture-based methods. Appl Environ Microbiol 68:4650–4652
14. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18
15. Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229
16. Berg G, Zachow C, Müller H, Philipps J, Tilcher R (2013) Next-generation bio-products sowing the seeds of success for sustainable agriculture. Agronomy 3:648–656
17. Berg G, Grube M, Schloter M, Smalla K (2014) The plant microbiome and its importance for plant and human health. Front Microbiol 5:491
18. Bionda N, Pitteloud JP, Cudic P (2013) Cyclic lipodepsipeptides: a new class of antibacterial agents in the battle against resistant bacteria. Future Med Chem 5:1311–1330
19. Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41
20. Cernava T (2012) Identification of volatile organic compounds from plant-associated bacteria. Graz University of Technology, Master thesis
21. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
22. Cotta SR, da Mota FF, Tupinambá G, Ishida K, Rozental S, Silva DO E, da Silva AJ, Bizzo HR, Alviano DS, Alviano CS, Seldin L (2012) Antimicrobial activity of Paenibacillus kribbensis POC 115 against the dermatophyte Trichophyton rubrum. World J Microbiol Biotechnol 28:953–962
23. Da Mota FF, Gomes EA, Seldin L (2008) Auxin production and detection of the gene coding for the Auxin Efflux Carrier (AEC) protein in Paenibacillus polymyxa. J Microbiol 46:257–264
24. Davies PJ (2010) Plant hormones: biosynthesis, signal transduction, action! 3rd edn. Springer, Dordrecht
25. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428–16433
26. Deng Y, Lu Z, Lu F, Wang Y, Bie X (2011a) Study on an antimicrobial protein produced by Paenibacillus polymyxa JSa-9 isolated from soil. World J Microbiol Biotechnol 27:1803–1807
27. Deng Y, Lu Z, Lu F, Zhang C, Wang Y, Zhao H, Bie X (2011b) Identification of LI-F type antibiotics and di-n-butyl phthalate produced by Paenibacillus polymyxa. J Microbiol Methods 85:175–182
28. Deng Y, Lu Z, Bi H, Lu F, Zhang C, Bie X (2011c) Isolation and characterization of peptide antibiotics LI-F04 and polymyxin B6 produced by Paenibacillus polymyxa strain JSa-9. Peptides 32:1917–1923
29. Ding Y, Wang J, Liu Y, Chen S (2005) Isolation and identification of nitrogen‐fixing bacilli from plant rhizospheres in Beijing region. J Appl Microbiol 99:1271–1281
30. Dobbelaere S, Croonenborghs A, Thys A, Broek AV, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:153–162
31. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. CRC Crit Rev Plant Sci 22:107–149
32. El-Deeb B, Fayez K, Gherbawy Y (2013) Isolation and characterization of endophytic bacteria from Plectranthus tenuiflorus medicinal plant in Saudi Arabia desert and their antimicrobial activities. J Plant Interact 8(1):56–64
33. Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol Lett 171:1–9
34. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G (2014) The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front Microbiol 5:175
35. Fürnkranz M, Lukesch B, Müller H, Huss H, Grube M, Berg G (2012a) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63:418–428
36. Fürnkranz M, Adam E, Müller H, Grube M, Huss H, Winkler J, Berg G (2012b) Promotion of growth, health and stress tolerance of Styrian oil pumpkins by bacterial endophytes. Eur J Plant Pathol 134:509–519
37. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103:10–19
38. Giamarellou H, Poulakou G (2009) Multidrug-resistant Gram-negative infections: what are the treatment options? Drugs 69:1879–1901
39. Govindasamy V, Senthilkumar M, Magheshwaran V, Kumar U, Bose P, Sharma V, Annapurna K (2011) Bacillus and Paenibacillus spp.: potential PGPR for sustainable agriculture. In: Maheshwari D (ed) Plant growth and health promoting bacteria; microbiology monographs 18. Springer, Berlin Heidelberg, pp 333–364
40. Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424
41. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914
42. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compante S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews, under revision
43. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14
44. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598
45. Heil M, Bostock RM (2002) Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann Bot 89:503–512
46. Holl FB, Chanway CP (1992) Rhizosphere colonization and seedling growth promotion of lodgepole pine by Bacillus polymyxa. Can J Microbiol 38:303–308
47. Ito M, Koyama Y (1972) Jolipeptin, a new peptide antibiotic. II. The mode of action of jolipeptin. J Antibiot 25:309–314
48. Jin HJ, Tu R, Xu F, Chen SF (2011) Identification of nitrogen-fixing Paenibacillus from different plant rhizospheres and a novel nifH gene detected in the P. stellifer. Microbiology 80:117–124
49. Kajimura Y, Kaneda M (1996) Fusaricidin A, a new depsipeptide antibiotic produced by Bacillus polymyxa KT-8. Taxonomy, fermentation, isolation, structure elucidation and biological activity. J Antibiot 49:129–135
50. Kajimura Y, Kaneda M (1997) Fusaricidins B, C and D, new depsipeptide antibiotics produced by Bacillus polymyxa KT-8: isolation, structure elucidation and biological activity. J Antibiot 50:220–228
51. Keita MB, Padhmananabhan R, Caputo A, Robert C, Delaporte E, Raoult D, Bittar F (2014) Non-contiguous finished genome sequence and description of Paenibacillus gorillae sp. nov. Stand Genomic Sci 9:1031–1045
52. Kim SB, Timmusk S (2013) A simplified method for Paenibacillus polymyxa gene knockout and insertional screening. PLoS ONE. doi:10.1371/journal.pone.0068092
53. Kimura Y, Murai E, Fujisawa M, Tatsuki T, Nobue F (1969) Polymyxin P, new antibiotics of polymyxin group. J Antibiot 22:449–450
54. Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, von Mering C, Vorholt JA (2011) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390
55. Köberl M, Müller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 6, e24452
56. Köberl M, Ramadan EM, Adam M, Cardinale M, Hallmann J, Heuer H, Smalla K, Berg G (2013) Bacillus and Streptomyces were selected as broad-spectrum antagonists against soilborne pathogens from arid areas in Egypt. FEMS Microbiol Lett 342:168–178
57. Krechel A, Faupel A, Hallmann J, Ulrich A, Berg G (2004) Potato-associated bacteria and their antagonistic potential towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can J Microbiol 48:772–786
58. Kurusu K, Ohba K, Arai T, Fukushima K (1987) New peptide antibiotics LI-F03, F04, F05, F07, and F08, produced by Bacillus polymyxa. I. Isolation and characterization. J Antibiot 40:1506–1514
59. Lal S, Tabacchioni S (2009) Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J Microbiol 49:2–10
60. Landman D, Georgescu C, Martin DA, Quale J (2008) Polymyxins revisited. Clin Microbiol Rev 21:449–465
61. Lebuhn M, Heulin T, Hartmann A (1997) Production of auxin and other indolic and phenolic compounds by Paenibacillus polymyxa strains isolated from different proximity to plant roots. FEMS Microbiol Ecol 22:325–334
62. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS One 7, e48744
63. Lehninger AL (1975) Biochemistry: the molecular basis of cell structure and function. Worth, New York
64. Liu WW, Mu W, Zhu BY, Du YC, Liu F (2008) Antagonistic activities of volatiles from four strains of Bacillus spp. and Paenibacillus spp. against soil-borne plant pathogens. Agric Sci China 7:1104–1114
65. Logares R, Sunagawa S, Salazar G, Cornejo‐Castillo FM, Ferrera I, Sarmento H, Hingamp P, Ogata H, de Vargas C, Lima-Mendez G, Raes J, Poulain J, Jaillon O, Wincker P, Kandels-Lewis S, Karsteni E, Acinas SG (2014) Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16:2659–2671
66. López D, Vlamakis H, Losick R, Kolter R (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618
67. Ludwig-Müller J (2014) Auxin homeostasis, signaling and interaction with other growth hormones during the clubroot disease of Brassicaceae. Plant Signal Behav 9, e28593
68. McSpadden Gardener BB (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94:1252–1258
69. Moissl-Eichinger C, Auerbach AK, Probst AJ, Mahnert A, Tom L, Piceno Y, Andersen GL, Venkateswaran K, Rettberg P, Barczyk S, Pukall R, Berg G (2015) Quo vadis? Microbial profiling revealed strong effects of cleanroom maintenance and routes of contamination in indoor environments. Sci Rep 5:9156
70. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012) Trichoderma-plant-pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52:522–529
71. Müller H, Berg C, Landa BB, Auerbach A, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front Microbiol 6:138
72. Nakajima N, Chihara S, Koyama Y (1972) A new antibiotic, gatavalin. I. Isolation and characterization. J Antibiot 25:243–247
73. Niu B, Vater J, Rueckert C, Blom J, Lehmann M, Ru JJ, Chen XH, Wang Q, Borriss R (2013) Polymyxin P is the active principle in suppressing phytopathogenic Erwinia spp. by the biocontrol rhizobacterium Paenibacillus polymyxa M-1. BMC Microbiol 13:137
74. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125
75. Pettersson B, Rippere KE, Yousten AA, Priest FG (1999) Transfer of Bacillus lentimorbus and Bacillus popilliae to the genus Paenibacillus with emended descriptions of Paenibacillus lentimorbus comb. nov. and Paenibacillus popilliae comb. nov. Int J Syst Bacteriol 49:531–540
76. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799
77. Pichard B, Larue JP, Thouvenot D (1995) Gavaserin and saltavalin, new peptide antibiotics produced by Bacillus polymyxa. FEMS Microbiol Lett 133:215–218
78. Raza W, Yang W, Shen QR (2008) Paenibacillus polymyxa: antibiotics, hydrolytic enzymes and hazard assessment. J Plant Pathol 90:419–430
79. Roh SW, Abell GC, Kim KH, Nam YD, Bae JW (2010) Comparing microarrays and next-generation sequencing technologies for microbial ecology research. Trends Biotechnol 28:291–299
80. Rybakova D, Schmuck M, Berg G (2015) Kill or cure? The interaction between endophytic Paenibacillus and Serratia spp. and the host plant is shaped by the environment; submitted
81. Sakiyama CC, Paula EM, Pereira PC, Borges AC, Silva DO (2001) Characterization of pectin lyase produced by an endophytic strain isolated from coffee cherries. Lett Appl Microbiol 33:117–121
82. Scherling C, Ulrich K, Ewald D, Weckwerth W (2009) A metabolic signature of the beneficial interaction of the endophyte Paenibacillus sp. isolate and in vitro-grown poplar plants revealed by metabolomics. Mol Plant Microbe Interact 22:1032–1037
83. Schmid F, Moser G, Müller H, Berg G (2011) Functional and structural microbial diversity in organic and conventional viticulture: organic farming benefits natural biocontrol agents. Appl Environ Microbiol 77:2188–2191
84. Schoina C, Stringlis IA, Pantelides IS, Tjamos SE, Paplomatas EJ (2011) Evaluation of application methods and biocontrol efficacy of Paenibacillus alvei strain K-165, against the cotton black root rot pathogen Thielaviopsis basicola. Biol Control 58:68–73
85. Shishido M, Loeb BM, Chanway CP (1995) External and internal root colonization of lodgepole pine seedlings by two growth-promoting Bacillus strains originated from different root microsites. Can J Microbiol 41:707–713
86. Shishido M, Massicotte HB, Chanway CP (1996) Effect of plant growth promoting Bacillus strains on pine and spruce seedling growth and mycorrhizal infection. Ann Bot 77:433–442
87. Shoji J, Hinoo H, Wakisaka Y, Koizumi K, Mayama M, Matsuura S (1977a) Isolation of two new polymyxin group antibiotics. (Studies on antibiotics from the genus Bacillus. X). J Antibiot 30:1029–1034
88. Shoji J, Kato T, Hinoo H (1977b) The structure of polymyxin S. (Studies on antibiotics from the genus Bacillus. XXI). J Antibiot (Tokyo) 30:1035–1041
89. Shoji J, Kato T, Hinoo H (1977c) The structure of polymyxin T1. (Studies on antibiotics from the genus Bacillus. XXII). J Antibiot 30:1042–1048
90. Smith EF (1911) Bacteria in relation to plant diseases. Carnegie Institute, Washington, USA
91. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism–plant signaling. FEMS Microbiol Rev 31:425–448
92. Stansly PG, Schlosser ME (1947) Studies on polymyxin: isolation and identification of Bacillus polymyxa and differentiation of polymyxin from certain known antibiotics. J Bacteriol 54:549
93. Timmusk S (2015) Sfp-type PPTase inactivation promotes bacterial biofilm formation and ability to enhance wheat drought tolerance. Front Microbiol 6:387
94. Timmusk S, Nevo E (2011) Plant root associated biofilms. In: Maheshwari DK (ed) Bacteria in 3 agrobiology. Plant nutrient management. Springer Verlag, Berlin 3:285–300
95. Timmusk S, Wagner EGH (1999) The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant-Microbe Interact 12:951–959
96. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852
97. Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71:7292–7300
98. Timmusk S, Paalme V, Lagercrantz U, Nevo E (2009) Detection and quantification of Paenibacillus polymyxa in the rhizosphere of wild barley (Hordeum spontaneum) with real-time PCR. J Appl Microbiol 107:736–745
99. Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T, Nevo E (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6, e17968
100. Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9, e96086
101. Tindall BJ (2000) What is the type species of the genus Paenibacillus? Request for an opinion. Int J Syst Evol Microbiol 50:939–940
102. Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561
103. Trüper HG (2005) The type species of the genus Paenibacillus Ash et al. 1994 is Paenibacillus polymyxa. Opinion 77. Int J Syst Evol Microbiol 55:17
104. Tupinambá G, Da Silva AJR, Alviano CS, Souto‐Padron TCBS, Seldin L, Alviano DS (2008) Antimicrobial activity of Paenibacillus polymyxa SCE2 against some mycotoxin‐producing fungi. J Appl Microbiol 105:1044–1053
105. Ulrich K, Stauber, Ewald D (2008a) Paenibacillus—a predominant endophytic bacterium colonising tissue cultures of woody plants. Plant Cell Tissue Organ Cult 93:347–351
106. Ulrich K, Ulrich A, Ewald D (2008b) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180
107. Van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci U S A 109:1159–1164
108. Verginer M, Leitner E, Berg G (2010) Production of volatile metabolites by grape-associated microorganisms. J Agric Food Chem 58:8344–8350
109. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168
110. Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256
111. Wilkinson S, Lowe LA (1966) Structures of the polymyxins A and the question of identity with the polymyxins M. Nature 212:311
112. Woolhouse M, Farrar J (2014) Policy: an intergovernmental panel on antimicrobial resistance. Nature 509:555–557
113. Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida CR12-2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71
114. Xie JB, Du Z, Bai L, Tian C, Zhang Y, Xie JY, Wang T, Liu X, Chen X, Cheng Q, Chen S, Li J (2014) Comparative genomic analysis of N2-fixing and non-N2-fixing Paenibacillus spp.: organization, evolution and expression of the nitrogen fixation genes. PLoS Genet 10, e1004231
115. Zhao LJ, Yang XN, Li XY, Mu W, Liu F (2011) Antifungal, insecticidal and herbicidal properties of volatile components from Paenibacillus polymyxa strain BMP-11. Agric Sci China 10:728–736
116. Zhou J, He Z, Yang Y, Deng Y, Tringe SG, Alvarez-Cohen L (2015) High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio 6:e02288–14