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Characterization of Lysobacter enzymogenes B25, a potential biological control agent of plant-parasitic nematodes, and its mode of action

  • Received: 09 December 2022 Revised: 16 February 2023 Accepted: 22 February 2023 Published: 01 March 2023
  • It is certainly difficult to estimate productivity losses due to the action of phytopathogenic nematodes but it might be about 12 % of world agricultural production. Although there are numerous tools to reduce the effect of these nematodes, there is growing concern about their environmental impact. Lysobacter enzymogenes B25 is an effective biological control agent against plant-parasitic nematodes, showing control over root-knot nematodes (RKN) such as Meloidogyne incognita and Meloidogyne javanica. In this paper, the efficacy of B25 to control RKN infestation in tomato plants (Solanum lycopersicum cv. Durinta) is described. The bacterium was applied 4 times at an average of concentration around 108 CFU/mL showing an efficacy of 50–95 % depending on the population and the pressure of the pathogen. Furthermore, the control activity of B25 was comparable to that of the reference chemical used. L. enzymogenes B25 is hereby characterized, and its mode of action studied, focusing on different mechanisms that include motility, the production of lytic enzymes and secondary metabolites and the induction of plant defenses. The presence of M. incognita increased the twitching motility of B25. In addition, cell-free supernatants obtained after growing B25, in both poor and rich media, showed efficacy in inhibiting RKN egg hatching in vitro. This nematicidal activity was sensitive to high temperatures, suggesting that it is mainly due to extracellular lytic enzymes. The secondary metabolites heat-stable antifungal factor and alteramide A/B were identified in the culture filtrate and their contribution to the nematicidal activity of B25 is discussed. This study points out L. enzymogenes B25 as a promising biocontrol microorganism against nematode infestation of plants and a good candidate to develop a sustainable nematicidal product.

    Citation: Sònia Martínez-Servat, Lola Pinyol-Escala, Oriol Daura-Pich, Marta Almazán, Iker Hernández, Belén López-García, Carolina Fernández. Characterization of Lysobacter enzymogenes B25, a potential biological control agent of plant-parasitic nematodes, and its mode of action[J]. AIMS Microbiology, 2023, 9(1): 151-176. doi: 10.3934/microbiol.2023010

    Related Papers:

  • It is certainly difficult to estimate productivity losses due to the action of phytopathogenic nematodes but it might be about 12 % of world agricultural production. Although there are numerous tools to reduce the effect of these nematodes, there is growing concern about their environmental impact. Lysobacter enzymogenes B25 is an effective biological control agent against plant-parasitic nematodes, showing control over root-knot nematodes (RKN) such as Meloidogyne incognita and Meloidogyne javanica. In this paper, the efficacy of B25 to control RKN infestation in tomato plants (Solanum lycopersicum cv. Durinta) is described. The bacterium was applied 4 times at an average of concentration around 108 CFU/mL showing an efficacy of 50–95 % depending on the population and the pressure of the pathogen. Furthermore, the control activity of B25 was comparable to that of the reference chemical used. L. enzymogenes B25 is hereby characterized, and its mode of action studied, focusing on different mechanisms that include motility, the production of lytic enzymes and secondary metabolites and the induction of plant defenses. The presence of M. incognita increased the twitching motility of B25. In addition, cell-free supernatants obtained after growing B25, in both poor and rich media, showed efficacy in inhibiting RKN egg hatching in vitro. This nematicidal activity was sensitive to high temperatures, suggesting that it is mainly due to extracellular lytic enzymes. The secondary metabolites heat-stable antifungal factor and alteramide A/B were identified in the culture filtrate and their contribution to the nematicidal activity of B25 is discussed. This study points out L. enzymogenes B25 as a promising biocontrol microorganism against nematode infestation of plants and a good candidate to develop a sustainable nematicidal product.



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    Conflict of interest



    The use of L. enzymogenes B25 as a biocontrol agent is subjected to a patent application. BLG, CF, IH, LPE, MA, ODP, and SMS were employed by Futureco Bioscience S.A.

    Author contributions:



    BLG and SMS conceived the work, contributed to the design and interpretation of the results and did the main writing of the article. CF, IH, LPE, and MA partially wrote specific sections. IH, LPE, MA, and ODP performed the experiments presented in the work and analyzed the data. CF supervised the work and revised the manuscript. All the authors have read the manuscript and agreed to its content.

    [1] Zhang ZQ (2013) Animal biodiversity: An update of classification and diversity in 2013. (Addenda 2013). Zootaxa 3703: 5-11. https://doi.org/10.11646/zootaxa.3703.1.3
    [2] Decraemer W, Hunt DJ (2006) Structure and classification. Plant nematology. Wallingford, UK; Cambridge, MA, USA: CABI 3-32. https://doi.org/10.1079/9781845930561.0003
    [3] Singh S, Singh B, Singh AP (2015) Nematodes: A threat to sustainability of agriculture. Procedia Environ Sci 29: 215-216. https://doi.org/10.1016/j.proenv.2015.07.270
    [4] Lima FSO, Mattos VS, Silva ES, et al. (2018) Nematodes affecting potato and sustainable practices for their management. Potato-From Incas to All Over the World. London: IntechOpen. https://doi.org/10.5772/intechopen.73056
    [5] Mantelin S, Bellafiore S, Kyndt T (2017) Meloidogyne graminicola: a major threat to rice agriculture. Mol Plant Pathol 18: 3-15. https://doi.org/10.1111/mpp.12394
    [6] Mesa-Valle CM, Garrido-Cardenas JA, Cebrian-Carmona J, et al. (2020) Global Research on Plant Nematodes. Agronomy 10: 1148. https://doi.org/10.3390/agronomy10081148
    [7] Sasanelli N, Konrat A, Migunova V, et al. (2021) Review on control methods against plant parasitic nematodes applied in southern member states (C Zone) of the European Union. Agriculture (Basel) 11. https://doi.org/10.3390/agriculture11070602
    [8] Kobayashi DY, Yuen GY (2005) The role of clp-regulated factors in antagonism against Magnaporthe poae and biological control of summer patch disease of Kentucky bluegrass by Lysobacter enzymogenes C3. Can J Microbiol 51: 719-723. https://doi.org/10.1139/w05-056
    [9] Han S, Shen D, Zhao Y, et al. (2018) Sigma factor RpoN employs a dual transcriptional regulation for controlling twitching motility and biofilm formation in Lysobacter enzymogenes OH11. Curr Genet 64: 515-527. https://doi.org/10.1007/s00294-017-0770-z
    [10] Zhao Y, Qian G, Chen Y, et al. (2017) Transcriptional and antagonistic responses of biocontrol strain Lysobacter enzymogenes OH11 to the plant pathogenic oomycete Pythium aphanidermatum. Front Microbiol 8: 1025. https://doi.org/10.3389/fmicb.2017.01025
    [11] Zhou M, Shen D, Xu G, et al. (2017) ChpA controls twitching motility and broadly affects gene expression in the biological control agent Lysobacter enzymogenes. Curr Microbiol 74: 566-574. https://doi.org/10.1007/s00284-017-1202-5
    [12] Patel N, Oudemans PV, Hillman BI, et al. (2013) Use of the tetrazolium salt MTT to measure cell viability effects of the bacterial antagonist Lysobacter enzymogenes on the filamentous fungus Cryphonectria parasitica. Antonie Van Leeuwenhoek 103: 1271-1280. https://doi.org/10.1007/s10482-013-9907-3
    [13] Chen J, Moore WH, Yuen GY, et al. (2006) Influence of Lysobacter enzymogenes Strain C3 on Nematodes. J Nematol 38: 233-239.
    [14] Yuen GY, Broderick KC, Jochum CC, et al. (2018) Control of cyst nematodes by Lysobacter enzymogenes strain C3 and the role of the antibiotic HSAF in the biological control activity. Biological Control 117: 158-163. https://doi.org/10.1016/j.biocontrol.2017.11.007
    [15] Xia J, Chen J, Chen Y, et al. (2018) Type IV pilus biogenesis genes and their roles in biofilm formation in the biological control agent Lysobacter enzymogenes OH11. Appl Microbiol Biotechnol 102: 833-846. https://doi.org/10.1007/s00253-017-8619-4
    [16] Xu K, Lin L, Shen D, et al. (2021) Clp is a ‘‘busy” transcription factor in the bacterial warrior, Lysobacter enzymogenes. Comput Struct Biotechnol J 19: 3564-3572. https://doi.org/10.1016/j.csbj.2021.06.020
    [17] Zhao Y, Jiang T, Xu H, et al. (2021) Characterization of Lysobacter spp. strains and their potential use as biocontrol agents against pear anthracnose. Microbiol Res 242: 126624. https://doi.org/10.1016/j.micres.2020.126624
    [18] Yu F, Zaleta-Rivera K, Zhu X, et al. (2007) Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimicrob Agents Chemother 51: 64-72. https://doi.org/10.1128/AAC.00931-06
    [19] Li S, Jochum CC, Yu F, et al. (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98: 695-701. https://doi.org/10.1094/PHYTO-98-6-0695
    [20] Li S, Calvo AM, Yuen GY, et al. (2009) Induction of cell wall thickening by the antifungal compound dihydromaltophilin disrupts fungal growth and is mediated by sphingolipid biosynthesis. J Eukaryot Microbiol 56: 182-187. https://doi.org/10.1111/j.1550-7408.2008.00384.x
    [21] Itoh H, Tokumoto K, Kaji T, et al. (2018) Total synthesis and biological mode of action of WAP-8294A2: A menaquinone-targeting antibiotic. J Org Chem 83: 6924-6935. https://doi.org/10.1021/acs.joc.7b02318
    [22] Odhiambo BO, Xu G, Qian G, et al. (2017) Evidence of an unidentified extracellular heat-stable factor produced by Lysobacter enzymogenes (OH11) that degrade Fusarium graminearum PH1 hyphae. Curr Microbiol 74: 437-448. https://doi.org/10.1007/s00284-017-1206-1
    [23] Choi H, Kim HJ, Lee JH, et al. (2012) Insight into genes involved in the production of extracellular chitinase in a biocontrol bacterium Lysobacter enzymogenes C-3. Plant Pathol J 28: 439-445. https://doi.org/10.5423/PPJ.NT.07.2012.0115
    [24] Kobayashi DY, Reedy RM, Palumbo JD, et al. (2005) A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3. Appl Environ Microbiol 71: 261-269. https://doi.org/10.1128/AEM.71.1.261-269.2005
    [25] Kilic-Ekici O, Yuen GY (2004) Comparison of strains of Lysobacter enzymogenes and PGPR for induction of resistance against Bipolaris sorokiniana in tall fescue. Biological Control 30: 446-455. https://doi.org/10.1016/j.biocontrol.2004.01.014
    [26] Kilic-Ekici O, Yuen GY (2003) Induced resistance as a mechanism of biological control by Lysobacter enzymogenes strain C3. Phytopathology 93: 1103-1110. https://doi.org/10.1094/PHYTO.2003.93.9.1103
    [27] Hernández I, Fernàndez C (2017) Draft genome sequence and assembly of a Lysobacter enzymogenes strain with biological control activity against root knot nematodes. Genome Announce 5: e00271-00217. https://doi.org/10.1128/genomeA.00271-17
    [28] Huedo P, Yero D, Martínez-Servat S, et al. (2014) Two different rpf clusters distributed among a population of Stenotrophomonas maltophilia clinical strains display differential diffusible signal factor production and virulence regulation. J Bacteriol 196: 2431-2442. https://doi.org/10.1128/JB.01540-14
    [29] Turnbull L, Whitchurch CB (2014) Motility assay: Twitching motility. Pseudomonas Methods and Protocols, Methods in Molecular Biology. New York: Springer Science+Business Media 73-86. https://doi.org/10.1007/978-1-4939-0473-0_9
    [30] Déziel E, Comeau Y, Villemur R (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204. https://doi.org/10.1128/JB.183.4.1195-1204.2001
    [31] Murthy N, Bleakley B (2012) Simplified method of preparing colloidal chitin used for screening of chitinase-producing microorganisms. Internet J Microbiol 10 Number 2. https://doi.org/10.5580/2bc3
    [32] Legesse DY (2017) Optimization and partial characterization of Bacillus protease isolated from soil and agro-industrial wastes. Int J Nutr Food Sci 6: 31-38. https://doi.org/10.11648/j.ijnfs.20170601.16
    [33] Ramnath L, Sithole B, Govinden R (2017) Identification of lipolytic enzymes isolated from bacteria indigenous to Eucalyptus wood species for application in the pulping industry. Biotechnol Rep 15: 114-124. https://doi.org/10.1016/j.btre.2017.07.004
    [34] Li H, Wu S, Wirth S, et al. (2014) Diversity and activity of cellulolytic bacteria, isolated from the gut contents of grass carp (Ctenopharyngodon idellus) (Valenciennes) fed on Sudan grass (Sorghum sudanense) or artificial feedstuffs. Aquacult Res 2014: 1-12. https://doi.org/10.1111/are.12478
    [35] de la Cruz TEE, Torres JMO (2012) Gelatin hydrolysis test protocol. Am Socr Microbiol : 1-10.
    [36] Kuiper I, Lagendijk EL, Pickford R, et al. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51: 97-113. https://doi.org/10.1046/j.1365-2958.2003.03751.x
    [37] Qian G, Wang Y, Liu Y, et al. (2013) Lysobacter enzymogenes uses two distinct cell-cell signaling systems for differential regulation of secondary-metabolite biosynthesis and colony morphology. Appl Environ Microbiol 79: 6604-6616. https://doi.org/10.1128/AEM.01841-13
    [38] Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
    [39] Song Y, Chen D, Lu K, et al. (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.00786
    [40] Song YY, Zeng RS, Xu JF, et al. (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5: e13324. https://doi.org/10.1371/journal.pone.0013324
    [41] Shabab M, Shindo T, Gu C, et al. (2008) Fungal effector protein AVR2 targets diversifying defense-related Cys proteases of tomato. Plant Cell 20: 1169-1183. https://doi.org/10.1105/tpc.107.056325
    [42] van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64: 251-263. https://doi.org/10.1007/s11103-007-9149-8
    [43] Pandey A, Misra P, Choudhary D, et al. (2015) AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues. Sci Rep 5: 12412. https://doi.org/10.1038/srep12412
    [44] Lin YM, Shih SL, Lin WC, et al. (2014) Phytoalexin biosynthesis genes are regulated and involved in plant response to Ralstonia solanacearum infection. Plant Sci 224: 86-94. https://doi.org/10.1016/j.plantsci.2014.04.008
    [45] Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55: 85-97. https://doi.org/10.1006/pmpp.1999.0213
    [46] Akbudak MA, Yildiz S, Filiz E (2020) Pathogenesis related protein-1 (PR-1) genes in tomato (Solanum lycopersicum L.): Bioinformatics analyses and expression profiles in response to drought stress. Genomics 112: 4089-4099.
    [47] Min D, Ai W, Zhou J, et al. (2020) SlARG2 contributes to MeJA-induced defense responses to Botrytis cinerea in tomato fruit. Pest Managet Sci 76: 3292-3301. https://doi.org/10.1002/ps.5888
    [48] Hwang IS, Oh EJ, Oh CS (2020) Transcriptional changes of plant defense-related genes in response to clavibacter infection in Pepper and Tomato. Plant Pathol J 36: 450-458. https://doi.org/10.5423/PPJ.OA.07.2020.0124
    [49] Yu XY, Bi Y, Yan L, et al. (2016) Activation of phenylpropanoid pathway and PR of potato tuber against Fusarium sulphureum by fungal elicitor from Trichothecium roseum. World J Microbiol Biotechnol 32: 142. https://doi.org/10.1007/s11274-016-2108-2
    [50] Douglas CJ, Hauffe KD, Ites-Morales ME, et al. (1991) Exonic sequences are required for elicitor and light activation of a plant defense gene, but promoter sequences are sufficient for tissue specific expression. Embo J 10: 1767-1775. https://doi.org/10.1002/j.1460-2075.1991.tb07701.x
    [51] Ellard-Ivey M, Douglas CJ (1996) Role of Jasmonates in the Elicitor- and Wound-Inducible Expression of Defense Genes in Parsley and Transgenic Tobacco. Plant Physiol 112: 183-192. https://doi.org/10.1104/pp.112.1.183
    [52] Fu J, Zhang S, Wu J, et al. (2020) Structural characterization of a polysaccharide from dry mycelium of Penicillium chrysogenum that induces resistance to Tobacco mosaic virus in tobacco plants. Int J Biol Macromol 156: 67-79. https://doi.org/10.1016/j.ijbiomac.2020.04.050
    [53] Ding Y, Li Y, Li Z, et al. (2016) Alteramide B is a microtubule antagonist of inhibiting Candida albicans. Biochim Biophys Acta 1860: 2097-2106. https://doi.org/10.1016/j.bbagen.2016.06.025
    [54] Tang B, Laborda P, Sun C, et al. (2019) Improving the production of a novel antifungal alteramide B in Lysobacter enzymogenes OH11 by strengthening metabolic flux and precursor supply. Bioresour Technol 273: 196-202. https://doi.org/10.1016/j.biortech.2018.10.085
    [55] Folman LB, Postma J, van Veen JA (2003) Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal diseases of cucumber. Microbiol Res 158: 107-115. https://doi.org/10.1078/0944-5013-00185
    [56] Gómez Expósito R, Postma J, Raaijmakers JM, et al. (2015) Diversity and activity of lysobacter species from disease suppressive soils. Front Microbiol 6: 1243. https://doi.org/10.3389/fmicb.2015.01243
    [57] Jochum CC, Osborne LE, Yuen GY (2006) Fusarium head blight biological control with Lysobacter enzymogenes strain C3. Biological Control 39: 336-344. https://doi.org/10.1016/j.biocontrol.2006.05.004
    [58] Talavera M (2003) Manual de nematologia agricola. Introducción al análisis y al control nematológico para agricultores y técnicos de agrupaciones de defensa vegetal. Conselleria d'Agricultura i Pesca de les Illes Balears .
    [59] Velmourougane K, Prasanna R, Saxena AK (2017) Agriculturally important microbial biofilms: Present status and future prospects. J Basic Microbiol 57: 548-573. https://doi.org/10.1002/jobm.201700046
    [60] Tomada S, Puopolo G, Perazzolli M, et al. (2016) Pea broth enhances the biocontrol efficacy of Lysobacter capsici AZ78 by triggering cell motility associated with biogenesis of type IV pilus. Front Microbiol 7: 1136. https://doi.org/10.3389/fmicb.2016.01136
    [61] Chen J, Shen D, Odhiambo BO, et al. (2018) Two direct gene targets contribute to Clp-dependent regulation of type IV pilus-mediated twitching motility in Lysobacter enzymogenes OH11. Appl Microbiol Biotechnol 102: 7509-7519. https://doi.org/10.1007/s00253-018-9196-x
    [62] Yang M, Ren S, Shen D, et al. (2020) ClpP mediates antagonistic interaction of Lysobacter enzymogenes with a crop fungal pathogen. Biological Control 140: 104125. https://doi.org/10.1016/j.biocontrol.2019.104125
    [63] Chen Y, Xia J, Su Z, et al. (2017) Lysobacter PilR, the regulator of type IV pilus synthesis, controls antifungal antibiotic production via a cyclic di-GMP pathway. Appl Environ Microbiol 83. https://doi.org/10.1128/AEM.03397-16
    [64] Zhou X, Qian G, Chen Y, et al. (2015) PilG is involved in the regulation of twitching motility and antifungal antibiotic biosynthesis in the biological control agent Lysobacter enzymogenes. Phytopathology 105: 1318-1324. https://doi.org/10.1094/PHYTO-12-14-0361-R
    [65] Hernández I, Sant C, Martínez R, et al. (2020) Design of bacterial strain-specific qPCR assays using NGS data and publicly available resources and its application to track biocontrol strains. Front Microbiol 11: 208. https://doi.org/10.3389/fmicb.2020.00208
    [66] Yang J, Liang L, Li J, et al. (2013) Nematicidal enzymes from microorganisms and their applications. Appl Microbiol Biotechnol 97: 7081-7095. https://doi.org/10.1007/s00253-013-5045-0
    [67] Duong B, Nguyen HX, Phan HV, et al. (2021) Identification and characterization of Vietnamese coffee bacterial endophytes displaying in vitro antifungal and nematicidal activities. Microbiol Res 242: 126613. https://doi.org/10.1016/j.micres.2020.126613
    [68] Nguyen XH, Naing KW, Lee YS, et al. (2013) Antagonistic potential of Paenibacillus elgii HOA73 against the root-knot nematode, Meloidogyne incognita. Nematology 15: 991-1000. https://doi.org/10.1163/15685411-00002737
    [69] Lee YS, Nguyen XH, Naing KW, et al. (2015) Role of lytic enzymes secreted by Lysobacter capsici YS1215 in the control of root-knot nematode of tomato plants. Indian J Microbiol 55: 74-80. https://doi.org/10.1007/s12088-014-0499-z
    [70] Lee YS, Park YS, Anees M, et al. (2013) Nematicidal activity of Lysobacter capsici YS1215 and the role of gelatinolytic proteins against root-knot nematodes. Biocontrol Sci Technol 23: 1427-1441. https://doi.org/10.1080/09583157.2013.840359
    [71] Mukhopadhyay RK D (2020) Trichoderma: a beneficial antifungal agent and insights into its mechanism of biocontrol potential. Egyptian J Biological Pest Control 30: 133. https://doi.org/10.1186/s41938-020-00333-x
    [72] Jamshidnejad V, Sahebani N, Etebarian H (2013) Potential biocontrol activity of Arthrobotrys oligospora and Trichoderma harzianum BI against Meloidogyne javanica on tomato in the greenhouse and laboratory studies. Arch Phytopathol Plant Prot 46: 1632-1640. https://doi.org/10.1080/03235408.2013.778476
    [73] Suarez B, Rey M, Castillo P, et al. (2004) Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl Microbiol Biotechnol 65: 46-55. https://doi.org/10.1007/s00253-004-1610-x
    [74] Castaneda-Alvarez C, Aballay E (2016) Rhizobacteria with nematicide aptitude: enzymes and compounds associated. World Microbiol Biotechnol 32: 203. https://doi.org/10.1007/s11274-016-2165-6
    [75] Aballay E, Prodan S, Zamorano A, et al. (2017) Nematicidal effect of rhizobacteria on plant-parasitic nematodes associated with vineyards. World J Microbiol Biotechnol 33: 131. https://doi.org/10.1007/s11274-017-2303-9
    [76] Sánchez Ortiz I, Alvarez Lugo I, Wong Padilla I, et al. (2018) Characterization of Cuban native bacteria isolated from nematodes as potential biological control agents for Meloidogyne spp. Rev Protección Veg 33: 1.
    [77] Han Y, Wang Y, Tombosa S, et al. (2015) Identification of a small molecule signaling factor that regulates the biosynthesis of the antifungal polycyclic tetramate macrolactam HSAF in Lysobacter enzymogenes. Appl Microbiol Biotechnol 99: 801-811. https://doi.org/10.1007/s00253-014-6120-x
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