Streptomyces and Bacillus species utilize volatile organic compounds to impact Fusarium oxysporum f.sp. vasinfectum race 4 (Fov4) virulence and suppress Fusarium wilt in Pima cotton

Emergence of a highly virulent Fusarium oxysporum f.sp. vasinfectum race 4 (Fov4) with aggressiveness towards Pima cotton (Gossypium barbadense) has raised significant concern for cotton producers while revealing challenges in soil-borne cotton disease management strategies which rely heavily on crop resistance and chemical controls. An alternative management approach uses antagonistic bacteria as biocontrol agents against Fov4. Initial studies showed a unique combination of bacteria Bacillus Rz141 and Streptomyces HC658 isolates displayed a mutualistic relationship capable of altering Fov4 growth. Notably, experimental design placed Fov4 between each isolate preventing direct physical contact of bacterial colonies. These observations led us to hypothesize that bacterial volatile organic compounds (VOCs) impact the growth and virulence of Fov4. Ensuring physical separation, I-plate cultures showed Rz141 had a VOC inhibition of 24%. Similarly, physically separated cultures of Rz141 and HC658 showed slight increase in VOC inhibition, 26% with some loss of Fov4 pigmentation. Pathogenicity assays where Fov4-infected Pima cotton was exposed to VOCs from physically separated Rz141 and HC658 showed VOCs can suppress Fov4 infection and reduce tissue darkening. Our results provide evidence that rhizosphere bacteria can use VOCs as a communication tool impacting fungal physiology and virulence, and ultimately Fov4-cotton interactions without direct physical contact.

[1]  Wen-Wen Zhou,et al.  Antifungal Activity of Volatile Organic Compounds Produced by Bacillus methylotrophicus and Bacillus thuringiensis against Five Common Spoilage Fungi on Loquats , 2020, Molecules.

[2]  A. Cherif,et al.  Isolation, Characterization and Chemical Synthesis of Large Spectrum Antimicrobial Cyclic Dipeptide (l-leu-l-pro) from Streptomyces misionensis V16R3Y1 Bacteria Extracts. A Novel 1H NMR Metabolomic Approach , 2020, Antibiotics.

[3]  C. Dunlap,et al.  Brevibacillus fortis NRS-1210 produces edeines that inhibit the in vitro growth of conidia and chlamydospores of the onion pathogen Fusarium oxysporum f. sp. cepae , 2020, Antonie van Leeuwenhoek.

[4]  R. Schwartz,et al.  Response to deficit irrigation of morphological, yield and fiber quality traits of upland (Gossypium hirsutum L.) and Pima (G. barbadense L.) cotton in the Texas High Plains , 2020 .

[5]  F. Reverchon,et al.  Diffusible and volatile organic compounds produced by avocado rhizobacteria exhibit antifungal effects against Fusarium kuroshium , 2020, Brazilian Journal of Microbiology.

[6]  A. Cao,et al.  Scent of a Killer: Microbial Volatilome and Its Role in the Biological Control of Plant Pathogens , 2020, Frontiers in Microbiology.

[7]  R. Nichols,et al.  First Report of Fusarium oxysporum f. sp. vasinfectum Race 4 Causing Fusarium Wilt of Cotton in New Mexico, U.S.A. , 2020 .

[8]  N. Magan,et al.  Efficacy of metabolites of a Streptomyces strain (AS1) to control growth and mycotoxin production by Penicillium verrucosum, Fusarium verticillioides and Aspergillus fumigatus in culture , 2020, Mycotoxin Research.

[9]  P. Schenk,et al.  Soil bacterial diffusible and volatile organic compounds inhibit Phytophthora capsici and promote plant growth. , 2019, The Science of the total environment.

[10]  Deng-bo Zhou,et al.  Taxonomy and Broad-Spectrum Antifungal Activity of Streptomyces sp. SCA3-4 Isolated From Rhizosphere Soil of Opuntia stricta , 2019, Front. Microbiol..

[11]  R. Nichols,et al.  Detection and Characterization of Fusarium oxysporum f. sp. vasinfectum VCG0114 (Race 4) Isolates of Diverse Geographic Origins. , 2019, Plant disease.

[12]  Matthew J. Gebert,et al.  A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by Actinobacteria , 2019, mSystems.

[13]  Alok R. Rai,et al.  Streptomyces from rotten wheat straw endowed the high plant growth potential traits and agro-active compounds , 2019, Biocatalysis and Agricultural Biotechnology.

[14]  A. Yousef,et al.  Antimicrobial peptides produced by Brevibacillus spp.: structure, classification and bioactivity: a mini review , 2018, World Journal of Microbiology and Biotechnology.

[15]  P. Roberts,et al.  Quantitative Trait Loci Mapping of Multiple Independent Loci for Resistance to Fusarium oxysporum f. sp. vasinfectum Races 1 and 4 in an Interspecific Cotton Population. , 2017, Phytopathology.

[16]  E. Santarém,et al.  Plant growth and resistance promoted by Streptomyces spp. in tomato. , 2017, Plant physiology and biochemistry : PPB.

[17]  R. Nichols,et al.  Genetic Diversity, Virulence, and Meloidogyne incognita Interactions of Fusarium oxysporum Isolates Causing Cotton Wilt in Georgia. , 2017, Plant disease.

[18]  Shiri Freilich,et al.  Prospects for Biological Soilborne Disease Control: Application of Indigenous Versus Synthetic Microbiomes. , 2017, Phytopathology.

[19]  A. Bell,et al.  Specific PCR Detection of Fusarium oxysporum f. sp. vasinfectum California Race 4 Based on a Unique Tfo1 Insertion Event in the PHO Gene. , 2017, Plant disease.

[20]  W. Jung,et al.  Antifungal activity of chitinase obtained from Paenibacillus ehimensis MA2012 against conidial of Collectotrichum gloeosporioides in vitro. , 2016, Microbial pathogenesis.

[21]  M. Petersen,et al.  Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. , 2016, FEMS microbiology ecology.

[22]  Roland Mumm,et al.  Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil , 2015, Front. Microbiol..

[23]  W. Raza,et al.  Effects of volatile organic compounds from Streptomyces albulus NJZJSA2 on growth of two fungal pathogens , 2015, Journal of basic microbiology.

[24]  T. Guo,et al.  Antifungal activity of Brevibacillus laterosporus JX-5 and characterization of its antifungal components , 2015, World Journal of Microbiology and Biotechnology.

[25]  G. Sacchetti,et al.  Diversity of food‐borne Bacillus volatile compounds and influence on fungal growth , 2015, Journal of applied microbiology.

[26]  R. Davis,et al.  Fusarium wilt of cotton: Management strategies , 2015 .

[27]  Yong Hwan Kim,et al.  Biocontrol of Fusarium wilt disease in tomato by Paenibacillus ehimensis KWN38 , 2015, World journal of microbiology & biotechnology.

[28]  I. Ivanova,et al.  Antibacterial potential of streptomycete strains from Antarctic soils , 2014, Biotechnology, biotechnological equipment.

[29]  L. Macías-Rodríguez,et al.  The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission , 2014, Plant and Soil.

[30]  C. Jeon,et al.  Diversity of the bacterial community in the rice rhizosphere managed under conventional and no-tillage practices , 2013, Journal of Microbiology.

[31]  M. Farag,et al.  Dynamic Chemical Communication between Plants and Bacteria through Airborne Signals: Induced Resistance by Bacterial Volatiles , 2013, Journal of Chemical Ecology.

[32]  W. Raza,et al.  Antifungal Activity of Bacillus amyloliquefaciens NJN-6 Volatile Compounds against Fusarium oxysporum f. sp. cubense , 2012, Applied and Environmental Microbiology.

[33]  R. Stipanovic,et al.  Phylogeny and pathogenicity of Fusarium oxysporum isolates from cottonseed imported from Australia into California for dairy cattle feed. , 2011, Canadian journal of microbiology.

[34]  M. Wei,et al.  Antifungal, Insecticidal and Herbicidal Properties of Volatile Components from Paenibacillus polymyxa Strain BMP-11 , 2011 .

[35]  Fengzhi Wu,et al.  Soil microbial community structure in cucumber rhizosphere of different resistance cultivars to fusarium wilt. , 2010, FEMS microbiology ecology.

[36]  M. Engel,et al.  Microbial community shifts in Pythium ultimum-inoculated suppressive substrates , 2008, Biology and Fertility of Soils.

[37]  R. Hutmacher,et al.  Characterization of California Isolates of Fusarium oxysporum f. sp. vasinfectum. , 2005, Plant disease.

[38]  S. Hong,et al.  Paenibacillus elgii sp. nov., with broad antimicrobial activity. , 2004, International journal of systematic and evolutionary microbiology.

[39]  I. Wilson,et al.  Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. , 2004, Molecular plant-microbe interactions : MPMI.

[40]  S. Molin,et al.  Volatile metabolites from actinomycetes. , 2002, Journal of agricultural and food chemistry.

[41]  K. O’Donnell,et al.  Evolution of Fusarium oxysporum f. sp. vasinfectum Races Inferred from Multigene Genealogies. , 2001, Phytopathology.

[42]  T. Parkin,et al.  Microbial Production of Volatile Organic Compounds in Soil Microcosms , 1996 .