Diversity and Activity of Lysobacter Species from Disease Suppressive Soils

The genus Lysobacter includes several species that produce a range of extracellular enzymes and other metabolites with activity against bacteria, fungi, oomycetes, and nematodes. Lysobacter species were found to be more abundant in soil suppressive against the fungal root pathogen Rhizoctonia solani, but their actual role in disease suppression is still unclear. Here, the antifungal and plant growth-promoting activities of 18 Lysobacter strains, including 11 strains from Rhizoctonia-suppressive soils, were studied both in vitro and in vivo. Based on 16S rRNA sequencing, the Lysobacter strains from the Rhizoctonia-suppressive soil belonged to the four species Lysobacter antibioticus, Lysobacter capsici, Lysobacter enzymogenes, and Lysobacter gummosus. Most strains showed strong in vitro activity against R. solani and several other pathogens, including Pythium ultimum, Aspergillus niger, Fusarium oxysporum, and Xanthomonas campestris. When the Lysobacter strains were introduced into soil, however, no significant and consistent suppression of R. solani damping-off disease of sugar beet and cauliflower was observed. Subsequent bioassays further revealed that none of the Lysobacter strains was able to promote growth of sugar beet, cauliflower, onion, and Arabidopsis thaliana, either directly or via volatile compounds. The lack of in vivo activity is most likely attributed to poor colonization of the rhizosphere by the introduced Lysobacter strains. In conclusion, our results demonstrated that Lysobacter species have strong antagonistic activities against a range of pathogens, making them an important source for putative new enzymes and antimicrobial compounds. However, their potential role in R. solani disease suppressive soil could not be confirmed. In-depth omics'–based analyses will be needed to shed more light on the potential contribution of Lysobacter species to the collective activities of microbial consortia in disease suppressive soils.

[1]  M. Christmann.  Bioactive natural products. , 2017, Bioorganic & medicinal chemistry.

[2]  P. Dorrestein,et al.  Comparative genomics and metabolic profiling of the genus Lysobacter , 2015, BMC Genomics.

[3]  Lysobacter tyrosinelyticus sp. nov. isolated from Gyeryongsan national park soil , 2015, Journal of Microbiology.

[4]  Hina Singh,et al.  Lysobacter fragariae sp. nov. and Lysobacterrhizosphaerae sp. nov. isolated from rhizosphere of strawberry plant , 2015, Antonie van Leeuwenhoek.

[5]  C. Young,et al.  Lysobacter lycopersici sp. nov., isolated from tomato plant Solanum lycopersicum , 2015, Antonie van Leeuwenhoek.

[6]  Kil-Yong Kim,et al.  Ovicidal activity of lactic acid produced by Lysobacter capsici YS1215 on eggs of root-knot nematode, Meloidogyne incognita. , 2014, Journal of microbiology and biotechnology.

[7]  P. Garbeva,et al.  Impact of interspecific interactions on antimicrobial activity among soil bacteria , 2014, Front. Microbiol..

[8]  R. Figueiredo,et al.  Fungal glycans and the innate immune recognition , 2014, Front. Cell. Infect. Microbiol..

[9]  I. Pertot,et al.  Lysobacter capsici AZ78 can be combined with copper to effectively control Plasmopara viticola on grapevine. , 2014, Microbiological research.

[10]  Jochen Wiesner,et al.  Biofilm-degrading enzymes from Lysobacter gummosus , 2014, Virulence.

[11]  L. Ledova,et al.  Lytic Peptidase L5 of Lysobacter sp. XL1 with Broad Antimicrobial Spectrum , 2014, Journal of Molecular Microbiology and Biotechnology.

[12]  C. Hertweck,et al.  Antibiotics from neglected bacterial sources. , 2014, International journal of medical microbiology : IJMM.

[13]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[14]  Yan Wang,et al.  Facile method for site-specific gene integration in Lysobacter enzymogenes for yield improvement of the anti-MRSA antibiotics WAP-8294A and the antifungal antibiotic HSAF. , 2013, ACS Synthetic Biology.

[15]  B. Piechulla,et al.  Bacterial Ammonia Causes Significant Plant Growth Inhibition , 2013, PloS one.

[16]  Yuemao Shen,et al.  Bioactive natural products from Lysobacter. , 2012, Natural product reports.

[17]  Identification of Traits Shared by Rhizosphere-Competent Strains of Fluorescent Pseudomonads , 2012, Microbial Ecology.

[18]  Yan Wang,et al.  Identification and Characterization of the Anti-Methicillin-Resistant Staphylococcus aureus WAP-8294A2 Biosynthetic Gene Cluster from Lysobacter enzymogenes OH11 , 2011, Antimicrobial Agents and Chemotherapy.

[19]  S. Hong,et al.  Investigation of Siderophore production and Antifungal activity against Phytophthora capsici as related to Iron (III) nutrition by Lysobacter antibioticus HS124 , 2011 .

[20]  P. Bakker,et al.  Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria , 2011, Science.

[21]  M. Afzal,et al.  Soil type affects plant colonization, activity and catabolic gene expression of inoculated bacterial strains during phytoremediation of diesel. , 2011, Journal of hazardous materials.

[22]  L. Eberl,et al.  Volatile-Mediated Killing of Arabidopsis thaliana by Bacteria Is Mainly Due to Hydrogen Cyanide , 2010, Applied and Environmental Microbiology.

[23]  K. Iwata,et al.  Ammonia accumulation in culture broth by the novel nitrogen-fixing bacterium, Lysobacter sp. E4. , 2010, Journal of bioscience and bioengineering.

[24]  J. Postma,et al.  Genotypic and phenotypic variation among Lysobacter capsici strains isolated from Rhizoctonia suppressive soils. , 2010, Systematic and applied microbiology.

[25]  J. Postma,et al.  Effect of successive cauliflower plantings and Rhizoctonia solani AG 2-1 inoculations on disease suppressiveness of a suppressive and a conducive soil , 2010 .

[26]  J. Postma,et al.  Specific detection of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8 with TaqMan® PCR , 2010, Journal of applied microbiology.

[27]  M. Habib.  Sugarbeet (Beta vulgaris L.) seed pre-treatment with water and HCl to improve germination. , 2010 .

[28]  A. Hayward,et al.  Stenotrophomonas and Lysobacter: ubiquitous plant‐associated gamma‐proteobacteria of developing significance in applied microbiology , 2010, Journal of applied microbiology.

[29]  A. Raio,et al.  Identification and charactherization of Lysobacter capsici strain PG4: a new plant health-promoting rhizobacterium. , 2010 .

[30]  B. Lugtenberg,et al.  Plant-growth-promoting rhizobacteria. , 2009, Annual review of microbiology.

[31]  H. Krishnan,et al.  Biocontrol Ability of Lysobacter antibioticus HS124 Against Phytophthora Blight Is Mediated by the Production of 4-Hydroxyphenylacetic Acid and Several Lytic Enzymes , 2009, Current Microbiology.

[32]  G. Wiegers,et al.  Biological control of Pythium aphanidermatum in cucumber with a combined application of Lysobacter enzymogenes strain 3.1T8 and chitosan , 2009 .

[33]  M. Gullino,et al.  Suppressiveness to Fusarium oxysporum f. sp. radicis lycopersici in re-used perlite and perlite–peat substrates in soilless tomatoes , 2009 .

[34]  I. de Bruijn,et al.  Regulation of Cyclic Lipopeptide Biosynthesis in Pseudomonas fluorescens by the ClpP Protease , 2008, Journal of bacteriology.

[35]  M. Madan,et al.  Growth and Sporulation of , 2009 .

[36]  H. Bouwmeester,et al.  Removal of phytotoxic compounds from torrefied grass fibres by plant-beneficial microorganisms. , 2008, FEMS microbiology ecology.

[37]  J. Postma,et al.  Soil suppressiveness and functional diversity of the soil microflora in organic farming systems , 2008 .

[38]  G. Ji,et al.  Biological control of rice bacterial blight by Lysobacter antibioticus strain 13-1 , 2008 .

[39]  K. Zaleta-Rivera,et al.  An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. , 2008, Phytopathology.

[40]  I. Kulaev,et al.  Extracellular yeast-lytic enzyme of the bacterium Lysobacter sp. XL 1 , 2008, Biochemistry (Moscow).

[41]  C. Jeon,et al.  Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. , 2008, International journal of systematic and evolutionary microbiology.

[42]  C. Fuqua,et al.  Biofilm formation by plant-associated bacteria. , 2007, Annual review of microbiology.

[43]  G. Bloemberg,et al.  Rhizosphere competence and the role of root colonization in biocontrol , 2007 .

[44]  Toshiaki Ito,et al.  Suppression of Damping-Off Disease in Host Plants by the Rhizoplane Bacterium Lysobacter sp. Strain SB-K88 Is Linked to Plant Colonization and Antibiosis against Soilborne Peronosporomycetes , 2005, Applied and Environmental Microbiology.

[45]  D. Kobayashi,et al.  Mutagenesis of beta-1,3-Glucanase Genes in Lysobacter enzymogenes Strain C3 Results in Reduced Biological Control Activity Toward Bipolaris Leaf Spot of Tall Fescue and Pythium Damping-Off of Sugar Beet. , 2005, Phytopathology.

[46]  P. Foster.  Stress responses and genetic variation in bacteria. , 2005, Mutation research.

[47]  R. Bally,et al.  Chemotaxis of free-living nitrogen-fixing bacteria towards maize mucilage , 1986, Plant and Soil.

[48]  V. Rossi,et al.  Growth and sporulation of Stemphylium vesicarium, the causal agent of brown spot of pear, on herb plants of orchard lawns , 2005, European Journal of Plant Pathology.

[49]  C. Fuqua,et al.  Biofilm formation in plant-microbe associations. , 2004, Current opinion in microbiology.

[50]  M. Klein,et al.  Production of antifungal compounds by Lysobacter enzymogenes isolate 3.1T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber , 2004 .

[51]  Jan LW Rademaker,et al.  Characterization of the diversity of ecologically important microbes by rep-PCR genomic fingerprinting. , 2004 .

[52]  D. R. Zeigler,et al.  Gene sequences useful for predicting relatedness of whole genomes in bacteria. , 2003, International journal of systematic and evolutionary microbiology.

[53]  G. Yuen,et al.  Induced Resistance as a Mechanism of Biological Control by Lysobacter enzymogenes Strain C3. , 2003, Phytopathology.

[54]  G. Zylstra,et al.  Taxonomic positioning of two biological control agents for plant diseases as Lysobacter enzymogenes based on phylogenetic analysis of 16S rDNA, fatty acid composition and phenotypic characteristics , 2003, Journal of applied microbiology.

[55]  B. Gerhardson,et al.  Suppression of wheat-seedling diseases caused by Fusarium culmorum and Microdochium nivale using bacterial seed treatment , 2003 .

[56]  L. B. Folman,et al.  Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal diseases of cucumber. , 2003, Microbiological research.

[57]  A. Guckert,et al.  Root Colonization by Inoculated Plant Growth-Promoting Rhizobacteria , 2001 .

[58]  J. Steadman,et al.  Bean rust biological control using bacterial agents , 2001 .

[59]  A. R. Penheiter,et al.  Chitinases from the Plant Disease Biocontrol Agent, Stenotrophomonas maltophilia C3. , 2001, Phytopathology.

[60]  B. Lugtenberg,et al.  Molecular determinants of rhizosphere colonization by Pseudomonas. , 2001, Annual review of phytopathology.

[61]  G. Yuen,et al.  The Role of Chitinase Production by Stenotrophomonas maltophilia Strain C3 in Biological Control of Bipolaris sorokiniana. , 2000, Phytopathology.

[62]  B. Lugtenberg,et al.  Bacterial traits and genes involved in rhizosphere colonization , 1999 .

[63]  P. Bakker,et al.  Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. , 1995 .

[64]  P. Bakker,et al.  Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens , 1995 .

[65]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[66]  K. B. Johnson.  Dose-response relationships and inundative biological control , 1994 .

[67]  H. Reichenbach.  The Genus Lysobacter , 1992 .

[68]  C. Bull.  Relationship between root colonization and suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strains 2-79 , 1991 .

[69]  D. Gross,et al.  Selection of fluorescent pseudomonads antagonistic to Erwinia carotovora and suppressive of potato seed piece decay , 1986 .

[70]  G. Payne,et al.  Cultural techniques and conditions influencing growth and sporulation of Cercospora zeae-maydis and lesion development in corn. , 1983 .

[71]  F. D. Cook,et al.  Lysobacter, a New Genus of Nonfruiting, Gliding Bacteria with a High Base Ratio , 1978 .