Genetic Basis and Expression Pattern Indicate the Biocontrol Potential and Soil Adaption of Lysobacter capsici CK09

Lysobacter species have attracted increasing attention in recent years due to their capacities to produce diverse secondary metabolites against phytopathogens. In this research, we analyzed the genomic and transcriptomic patterns of Lysobacter capsici CK09. Our data showed that L. capsici CK09 harbored various contact-independent biocontrol traits, such as fungal cell wall lytic enzymes and HSAF/WAP-8294A2 biosynthesis, as well as several contact-dependent machineries, including type 2/4/6 secretion systems. Additionally, a variety of hydrolytic enzymes, particularly extracellular enzymes, were found in the L. capsici CK09 genome and predicted to improve its adaption in soil. Furthermore, several systems, including type 4 pili, type 3 secretion system and polysaccharide biosynthesis, can provide a selective advantage to L. capsici CK09, enabling the species to live on the surface in soil. The expression of these genes was then confirmed via transcriptomic analysis, indicating the activities of these genes. Collectively, our research provides a comprehensive understanding of the biocontrol potential and soil adaption of L. capsici CK09 and implies the potential of this strain for application in the future.

[1]  G. K. Upamanya,et al.  Molecular interaction between plants and Trichoderma species against soil-borne plant pathogens , 2023, Frontiers in Plant Science.

[2]  E. Piombo,et al.  Verticillium longisporum phospholipase VlsPLA 2 is a virulence factor that targets host nuclei and modulates plant immunity , 2023, Molecular Plant Pathology.

[3]  E. A. Barka,et al.  Modes of Action of Biocontrol Agents and Elicitors for sustainable Protection against Bacterial Canker of Tomato , 2023, Microorganisms.

[4]  Eirini G. Poulaki,et al.  Bacillus species: a factory of plant protective volatile organic compounds. , 2023, Journal of applied microbiology.

[5]  M. G. Garnica-Romo,et al.  Streptomyces spp. Biofilmed Solid Inoculant Improves Microbial Survival and Plant-Growth Efficiency of Triticum aestivum , 2022, Applied Sciences.

[6]  N. Gow,et al.  Architecture of the dynamic fungal cell wall , 2022, Nature Reviews Microbiology.

[7]  Shuzhen Wei,et al.  Lysobacter selenitireducens sp. nov., isolated from river sediment. , 2022, International journal of systematic and evolutionary microbiology.

[8]  I. Islas-Flores,et al.  Microbial Effectors: Key Determinants in Plant Health and Disease , 2022, Microorganisms.

[9]  M. Burmølle,et al.  The biofilm life cycle: expanding the conceptual model of biofilm formation , 2022, Nature Reviews Microbiology.

[10]  M. Mellata,et al.  Models for Gut-Mediated Horizontal Gene Transfer by Bacterial Plasmid Conjugation , 2022, Frontiers in Microbiology.

[11]  K. Feng,et al.  Biofilm Structural and Functional Features on Microplastic Surfaces in Greenhouse Agricultural Soil , 2022, Sustainability.

[12]  O. Alegbeleye,et al.  Impact of temperature, soil type and compost amendment on the survival, growth and persistence of Listeria monocytogenes of non-environmental (food-source associated) origin in soil. , 2022, The Science of the total environment.

[13]  G. Wong,et al.  The Power of Touch: Type 4 Pili, the von Willebrand A Domain, and Surface Sensing by Pseudomonas aeruginosa , 2022, Journal of bacteriology.

[14]  A. Filloux Bacterial protein secretion systems: Game of types. , 2022, Microbiology.

[15]  K. Machera,et al.  Evaluation of plant protection efficacy in field conditions and side effects of Lysobacter capsici AZ78, a biocontrol agent of Plasmopara viticola , 2022, Biocontrol Science and Technology.

[16]  Jianming Xu,et al.  Biochar alleviated the toxicity of atrazine to soybeans, as revealed by soil microbial community and the assembly process. , 2022, The Science of the total environment.

[17]  Surajit Das,et al.  Genetic regulation, biosynthesis and applications of extracellular polysaccharides of the biofilm matrix of bacteria. , 2022, Carbohydrate polymers.

[18]  W. Ahmed,et al.  Exploiting the antibacterial mechanism of phenazine substances from Lysobacter antibioticus 13-6 against Xanthomonas oryzae pv. oryzicola , 2022, Journal of Microbiology.

[19]  Hui Yang,et al.  Majorbio Cloud: A one‐stop, comprehensive bioinformatic platform for multiomics analyses , 2022, iMeta.

[20]  Jiawen Du,et al.  Evaluating the Mode of Antifungal Action of Heat-Stable Antifungal Factor (HSAF) in Neurospora crassa , 2022, Journal of fungi.

[21]  Yimin Zhang,et al.  Confirmation of the Need for Reclassification of Neisseria mucosa and Neisseria sicca Using Average Nucleotide Identity Blast and Phylogenetic Analysis of Whole-Genome Sequencing: Hinted by Clinical Misclassification of a Neisseria mucosa Strain , 2022, Frontiers in Microbiology.

[22]  E. Hoiczyk,et al.  A noncanonical cytochrome c stimulates calcium binding by PilY1 for type IVa pili formation , 2022, Proceedings of the National Academy of Sciences.

[23]  L. Du,et al.  Biosynthesis, regulation, and engineering of natural products from Lysobacter. , 2022, Natural product reports.

[24]  Konstantinos D. Tsirigos,et al.  SignalP 6.0 predicts all five types of signal peptides using protein language models , 2022, Nature Biotechnology.

[25]  Xiaobing Yang,et al.  Roles of Type VI Secretion System in Transport of Metal Ions , 2021, Frontiers in Microbiology.

[26]  J. Choudhary,et al.  The type III secretion system effector network hypothesis. , 2021, Trends in microbiology.

[27]  F. Short,et al.  The molecular basis of FimT-mediated DNA uptake during bacterial natural transformation , 2021, bioRxiv.

[28]  Y. Jo,et al.  The Role of Lysobacter antibioticus HS124 on the Control of Fall Webworm (Hyphantria cunea Drury) and Growth Promotion of Canadian Poplar (Populus canadensis Moench) at Saemangeum Reclaimed Land in Korea , 2021, Microorganisms.

[29]  S. Chou,et al.  Lysobacter enzymogenes antagonizes soilborne bacteria using the type IV secretion system. , 2021, Environmental microbiology.

[30]  Alexander M. Kloosterman,et al.  antiSMASH 6.0: improving cluster detection and comparison capabilities , 2021, Nucleic Acids Res..

[31]  K. Lewis,et al.  Biosynthesis and Mechanism of Action of the Cell Wall Targeting Antibiotic Hypeptin , 2021, Angewandte Chemie.

[32]  K. Makabe,et al.  Cloning, expression, and characterization of a GH 19-type chitinase with antifungal activity from Lysobacter sp. MK9-1. , 2020, Journal of bioscience and bioengineering.

[33]  R. Schuhmacher,et al.  Volatile-Mediated Inhibitory Activity of Rhizobacteria as a Result of Multiple Factors Interaction: The Case of Lysobacter capsici AZ78 , 2020, Microorganisms.

[34]  I. Toropygin,et al.  β-Lytic Protease of Lysobacter capsici VKM B-2533T , 2020, Antibiotics.

[35]  L. E. del Río Mendoza,et al.  Associations among the communities of soil-borne pathogens, soil edaphic properties and disease incidence in the field pea root rot complex , 2020, Plant and Soil.

[36]  Fengquan Liu,et al.  Characterization of Lysobacter spp. strains and their potential use as biocontrol agents against pear anthracnose. , 2020, Microbiological research.

[37]  Chaohui Li,et al.  Biocontrol ability and action mechanism of dihydromaltophilin against Colletotrichum fructicola causing anthracnose of pear fruit. , 2020, Pest management science.

[38]  S. Chou,et al.  An intrinsic mechanism for coordinated production of the contact-dependent and contact-independent weapon systems in a soil bacterium , 2020, PLoS pathogens.

[39]  L. Du,et al.  Identification of the biosynthetic gene cluster for the anti-MRSA lysocins through gene cluster activation using strong promoters of housekeeping genes and production of new analogs in Lysobacter sp. 3655. , 2020, ACS synthetic biology.

[40]  S. Coulthurst,et al.  Type VI secretion system effector proteins: effective weapons for bacterial competitiveness. , 2020, Cellular microbiology.

[41]  L. Yuan,et al.  Lysobacter enzymogenes LE16 autolysates have potential as biocontrol agents—Lysobacter sp. autolysates as biofungicide , 2020, Journal of applied microbiology.

[42]  J. G. Pontes,et al.  Virulence Factors in the Phytopathogen-Host Interactions: An Overview. , 2020, Journal of agricultural and food chemistry.

[43]  Fengquan Liu,et al.  Lysobacter gummosus OH17 induces systemic resistance in Oryza sativa ‘Nipponbare’ , 2020 .

[44]  B. Erni,et al.  Transporters of glucose and other carbohydrates in bacteria , 2020, Pflügers Archiv - European Journal of Physiology.

[45]  J. Whitney,et al.  Contact-Dependent Interbacterial Antagonism Mediated by Protein Secretion Machines. , 2020, Trends in microbiology.

[46]  Jincai Ma,et al.  Interaction between Fungal Communities, Soil Properties, and the Survival of Invading E. coli O157:H7 in Soils , 2020, International journal of environmental research and public health.

[47]  A. Cimmino,et al.  Isolation of 2,5-diketopiperazines from Lysobacter capsici AZ78 with activity against Rhodococcus fascians , 2020, Natural product research.

[48]  P. Vandamme,et al.  A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. , 2020, International journal of systematic and evolutionary microbiology.

[49]  K. Bush,et al.  Epidemiology of β-Lactamase-Producing Pathogens , 2020, Clinical Microbiology Reviews.

[50]  M. Artola,et al.  An overview of activity-based probes for glycosidases. , 2019, Current opinion in chemical biology.

[51]  J. Qiao,et al.  Characterization of Lysobacter capsici strain NF87–2 and its biocontrol activities against phytopathogens , 2019, European Journal of Plant Pathology.

[52]  A. Gómez-Cadenas,et al.  Root exudates: from plant to rhizosphere and beyond , 2019, Plant Cell Reports.

[53]  I. Henderson,et al.  The Type III Secretion System (T3SS)-Translocon of Atypical Enteropathogenic Escherichia coli (aEPEC) Can Mediate Adherence , 2019, Front. Microbiol..

[54]  N. Cianciotto,et al.  Assessing the impact, genomics and evolution of type II secretion across a large, medically important genus: the Legionella type II secretion paradigm , 2019, Microbial genomics.

[55]  Maxuel O. Andrade,et al.  Bactericidal type IV secretion system homeostasis in Xanthomonas citri , 2019, bioRxiv.

[56]  B. Maier,et al.  Type IV pili: dynamics, biophysics and functional consequences , 2019, Nature Reviews Microbiology.

[57]  A. Phillippy,et al.  High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries , 2018, Nature Communications.

[58]  J. V. van Elsas,et al.  Mechanisms and ecological implications of the movement of bacteria in soil , 2018, Applied Soil Ecology.

[59]  B. P. Jain,et al.  WD40 Repeat Proteins: Signalling Scaffold with Diverse Functions , 2018, The Protein Journal.

[60]  Alex Bateman,et al.  Non‐Coding RNA Analysis Using the Rfam Database , 2018, Current protocols in bioinformatics.

[61]  Shruthi Hamsanathan,et al.  The Tat protein transport system: intriguing questions and conundrums. , 2018, FEMS microbiology letters.

[62]  C. Pieterse,et al.  Emerging microbial biocontrol strategies for plant pathogens. , 2018, Plant science : an international journal of experimental plant biology.

[63]  I. Pertot,et al.  The impact of the omics era on the knowledge and use of Lysobacter species to control phytopathogenic micro‐organisms , 2018, Journal of applied microbiology.

[64]  Wenhao Yang,et al.  Variations of Escherichia coli O157:H7 Survival in Purple Soils , 2017, International journal of environmental research and public health.

[65]  T. Paulitz,et al.  Disease Suppressive Soils: New Insights from the Soil Microbiome. , 2017, Phytopathology.

[66]  Ashutosh Kumar Singh,et al.  Microbial taxonomy in the era of OMICS: application of DNA sequences, computational tools and techniques , 2017, Antonie van Leeuwenhoek.

[67]  J. Thomassin,et al.  The trans‐envelope architecture and function of the type 2 secretion system: new insights raising new questions , 2017, Molecular microbiology.

[68]  J. V. van Elsas,et al.  Role of flagella and type four pili in the co-migration of Burkholderia terrae BS001 with fungal hyphae through soil , 2017, Scientific Reports.

[69]  Shi-dong Li,et al.  Transformation of the endochitinase gene Chi67-1 in Clonostachys rosea 67-1 increases its biocontrol activity against Sclerotinia sclerotiorum , 2017, AMB Express.

[70]  S. Karamanou,et al.  Protein export through the bacterial Sec pathway , 2016, Nature Reviews Microbiology.

[71]  J. V. van Elsas,et al.  Chemotaxis and adherence to fungal surfaces are key components of the behavioral response of Burkholderia terrae BS001 to two selected soil fungi. , 2016, FEMS microbiology ecology.

[72]  J. V. van Elsas,et al.  The type three secretion system facilitates migration of Burkholderia terrae BS001 in the mycosphere of two soil-borne fungi , 2016, Biology and Fertility of Soils.

[73]  Zhenyu Jin,et al.  Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability , 2016, npj Biofilms and Microbiomes.

[74]  K. Engelen,et al.  The Lysobacter capsici AZ78 Genome Has a Gene Pool Enabling it to Interact Successfully with Phytopathogenic Microorganisms and Environmental Factors , 2016, Front. Microbiol..

[75]  Jörg Peplies,et al.  JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison , 2015, Bioinform..

[76]  J. Postma,et al.  Diversity and Activity of Lysobacter Species from Disease Suppressive Soils , 2015, Front. Microbiol..

[77]  L. Ting,et al.  Expression of Paenibacillus polymyxa β-1,3-1,4-glucanase in Streptomyces lydicus A01 improves its biocontrol effect against Botrytis cinerea , 2015 .

[78]  Y. Lai,et al.  The role of pgaC in Klebsiella pneumoniae virulence and biofilm formation. , 2014, Microbial pathogenesis.

[79]  L. Burrows,et al.  Pseudomonas aeruginosa Minor Pilins Prime Type IVa Pilus Assembly and Promote Surface Display of the PilY1 Adhesin* , 2014, The Journal of Biological Chemistry.

[80]  Stephen J. Wright,et al.  Biosynthetic Mechanism for Sunscreens of the Biocontrol Agent Lysobacter enzymogenes , 2013, PloS one.

[81]  L. Bai,et al.  Construction of Streptomyces lydicus A01 transformant with the chit33 gene from Trichoderma harzianum CECT2413 and its biocontrol effect on Fusaria , 2013 .

[82]  I. Kulaev,et al.  Cloning and Expression Analysis of Genes Encoding Lytic Endopeptidases L1 and L5 from Lysobacter sp. Strain XL1 , 2012, Applied and Environmental Microbiology.

[83]  J. Tiedje,et al.  Microbial Communities Associated with Potato Common Scab-Suppressive Soil Determined by Pyrosequencing Analyses. , 2012, Plant disease.

[84]  Antonio Di Pietro,et al.  The Top 10 fungal pathogens in molecular plant pathology. , 2012, Molecular plant pathology.

[85]  G. Salmond,et al.  N-Acetylglucosamine-dependent biofilm formation in Pectobacterium atrosepticum is cryptic and activated by elevated c-di-GMP levels. , 2012, Microbiology.

[86]  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.

[87]  K. Zaleta-Rivera,et al.  Biosynthesis of HSAF, a tetramic acid-containing macrolactam from Lysobacter enzymogenes. , 2011, Journal of the American Chemical Society.

[88]  R. Rosselló-Móra,et al.  Shifting the genomic gold standard for the prokaryotic species definition , 2009, Proceedings of the National Academy of Sciences.

[89]  M. Silby,et al.  Requirement of Polyphosphate by Pseudomonas fluorescens Pf0-1 for Competitive Fitness and Heat Tolerance in Laboratory Media and Sterile Soil , 2009, Applied and Environmental Microbiology.

[90]  M. Perry,et al.  Poly-N-acetylglucosamine mediates biofilm formation and antibiotic resistance in Actinobacillus pleuropneumoniae. , 2007, Microbial pathogenesis.

[91]  Peter F. Hallin,et al.  RNAmmer: consistent and rapid annotation of ribosomal RNA genes , 2007, Nucleic acids research.

[92]  K. Zaleta-Rivera,et al.  Structure and Biosynthesis of Heat-Stable Antifungal Factor (HSAF), a Broad-Spectrum Antimycotic with a Novel Mode of Action , 2006, Antimicrobial Agents and Chemotherapy.

[93]  L. Du,et al.  Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. , 2005, Molecular biology of the cell.

[94]  Youfu Zhao,et al.  Lysobacter enzymogenes strain C3 suppresses mycelium growth and spore germination of eight soybean fungal and oomycete pathogens and decreases disease incidences , 2021 .

[95]  Patricia P. Chan,et al.  tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. , 2019, Methods in molecular biology.

[96]  Honghui Zhu,et al.  Lysobacter silvisoli sp. nov., isolated from forest soil. , 2019, International journal of systematic and evolutionary microbiology.

[97]  Fengquan Liu,et al.  Type IV pilus biogenesis genes and their roles in biofilm formation in the biological control agent Lysobacter enzymogenes OH11 , 2017, Applied Microbiology and Biotechnology.

[98]  A. Mills Keeping in Touch: Microbial Life on Soil Particle Surfaces , 2003 .