Skip to main content
Log in

De novo genome sequencing of mycoparasite Mycogone perniciosa strain MgR1 sheds new light on its biological complexity

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Mycogone perniciosa is a mycoparasite causing Wet Bubble Diseases (WBD) of Agaricus bisporus. In the present study, the whole genome of M. perniciosa strain MgR1 was sequenced using Illumina NextSeq500 platform. This sequencing generated 8.03 Gb of high-quality data and a draft genome of 39 Mb was obtained through a de novo assembly of the high-quality reads. The draft genome resulted into prediction of 9276 genes from the 1597 scaffolds. NCBI-based homology analysis revealed the identification of 8660 genes. Notably, non-redundant protein database analysis of the M. perniciosa strain MgR1 revealed its close relation with the Trichoderma arundinaceum. Moreover, ITS-based phylogenetic analysis showed the highest similarity of M. perniciosa strain MgR1 with Hypomyces perniciosus strain CBS 322.22 and Mycogone perniciosa strain PPRI 5784. Annotation of the 3917 genes of M. perniciosa strain MgR1 grouped in three major categories viz. biological process (2583 genes), cellular component (2013 genes), and molecular function (2919 genes). UniGene analysis identified 2967 unique genes in M. perniciosa strain MgR1. In addition, prediction of the secretory and pathogenicity-related genes based on the fungal database indicates that 1512 genes (16% of predicted genes) encode for secretory proteins. Moreover, out of 9276 genes, 1296 genes were identified as pathogenesis-related proteins matching with 51 fungal and bacterial genera. Overall, the key pathogenic genes such as lysine M protein domain genes, G protein, hydrophobins, and cytochrome P450 were also observed. The draft genome of MgR1 provides an understanding of pathogenesis of WBD in A. bisporus and could be utilized to develop novel management strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The whole genome shotgun project has been deposited at NCBI under the accession numbers PRJNA543984. The version described in this paper is version PRJNA543984. The NCBI accession number of bio-sample is SAMN11793478 and ID is 11793478.

References

  1. Sharma VP, Annepu SK, Yogesh Y, Singh M, Kamal S (2017) Status of mushroom production in India. Mushroom Res 26:111–120

    Google Scholar 

  2. Sharma VP, Kumar S, Kamal S (2017) Management of wet bubble disease (Mycogone Perniciosa) in Agaricus bisporus. Mushroom Res 26:181–191

  3. Sharma SR, Kumar S, Sharma VP (2007) Diseases and competitor moulds of mushrooms and their management. Tech Bull NRCM. 1–81

  4. Sharma SR (1994) Survey for diseases in cultivated mushrooms. Annual Rep NRCM. 23

  5. Bhat N, Singh RP (2000) Incidence and loss in yield by fungal pathogens encountered from the beds of A. bisporus. Indian J Mushroom 18:46–49

    Google Scholar 

  6. Sharma SR, Kumar S (2000) Studies on wet bubble disease of white button mushroom, A. bisporus caused by M. perniciosa. Mushroom Sci 15:569–575

    Google Scholar 

  7. Kouser S, Shah M, Ahmed MD, Shah PA (2015) Sheikh morphological characteristics of wet bubble disease (Mycogone Perniciosa) isolated from button mushroom (Agaricus bisporus) and assessment of factors affecting disease development and spread. Afr J Microbiol Res 9:185–193

    Google Scholar 

  8. Fu Y, Wang X, Li D, Liu Y, Song B, Zhang C, Wang Q, Chen M, Zhang Z, Li Y (2016) Identification of resistance to wet bubble disease and genetic diversity in wild and cultivated strains of Agaricus bisporus. Int J Mol Sci 17:1–12

    Google Scholar 

  9. Nielsen O (1932). Mushroom diseases. Reprinted from Gartnertidende, 2p

  10. Glamoclija J, Sokovic M, Ljaljevic-Grbic M, Vukojevic J, Milenkovic I, Van Griensven L (2008) Morphological characteristics and mycelial compatibility of different Mycogone perniciosa isolates. J Microsc 232:489–492

    CAS  PubMed  Google Scholar 

  11. Fletcher JT, Jaffe B (1995) Muthumeenakshi S, Brown AE, Wright, DM, Variations in isolates of Mycogone perniciosa and in disease symptoms in Agaricus bisporus. Plant Pathol 44:130–140

    Google Scholar 

  12. Umar MH, Geels FP, Van Griensven LJLD (2000) Pathology and pathogenesis of Mycogone perniciosa infection in Agaricus bisporus. Mushroom Sci 15:561–568

    Google Scholar 

  13. Regnier T, Combrinck S (2010) vitro and in vivo screening of essential oils for the control of wet bubble disease of Agaricus bisporus. S Afr J Bot 76(4):681–685

    CAS  Google Scholar 

  14. Santos TLD, Belan LL, Zied DC, Dias ES, Alves E (2017) Essential oils in the control of dry bubble disease in white button mushroom. Ciencia Rural, Santa Maria 47(05):e20160780. https://doi.org/10.1590/0103-8478cr20160780

    Article  CAS  Google Scholar 

  15. Gea FJ, Tello, BJC, Navarro, MJ (2010) Efficacy and effects on yield of different fungicides for control of wet bubble. Crop Protect 29:1021e1025

  16. Szumigaj-Tarnowska J, Slusarski C, Ulinski Z (2015) Pathogenicity of Mycogone perniciosa isolates collected on polish mushroom farms. J Horticult Res 23:87–92

    Google Scholar 

  17. Zhang CL, Xu JZ, Kakishima M, Li Y (2017) First report of wet bubble disease caused by Hypomyces perniciosus on Pleurotus citrinopileatus in China. Plant Dis 101:1321

    Google Scholar 

  18. Zhou C, Li D, Chen L, Li Y (2016) Genetic diversity analysis of Mycogone perniciosa causing wet bubble disease of Agaricus bisporus in China using srap. J Phytopathol 164:271–275

    Google Scholar 

  19. Kaul TN, Kachroo JL, Ahmed N (1978) Diseases and competitors of mushroom farms in Kashmir Valley. Indian Mushroom Science 1:193–203

    Google Scholar 

  20. Baars J, Hendrickx P, Sonnenberg A. Korsten L (2013) Global collection of mushroom pathogens. Plant Research International, part of Wageningen UR Business Unit Plant Breeding Report 2013–1. 1–25pp. https://www.wageningenUR.nl/en/pri

  21. Geels FP, Van de Geijn J, Rutjens AJ (1988) Pests and Diseases. In The Cultivation of Mushrooms. (ed. L. J. L. D. Van Griensven), Darlington Mushroom Laboratories Ltd: Rustington, U.K. pp. 417–418

  22. Fletcher JT, Gaze RH (2007) Mushroom pest and disease control – a colour handbook. Manson Publishing Ltd, London

    Google Scholar 

  23. Kumar A, Sharma VP, Kumar S (2020) Mycoparasitism of Mycogone perniciosa in edible fungi. Agriallis 2(9):1–6

    Google Scholar 

  24. Fletcher JT, Gaze RH (2008) Mushroom pest and disease control: a color, handbook. Manson Publishing Ltd., Academic Press, San Diego

    Google Scholar 

  25. Choudhary DK, Agarwal PK, Johri BN (2009) Characterization of functional activity in composted casing amendments used in cultivation of Agaricus bisporus (Lange) Imbach. Indian J Biotechnol 8(1):97–109

    CAS  Google Scholar 

  26. Carrasco J, Preston GM (2020) Growing edible mushrooms: a conversation between bacteria and fungi. Environ Microbiol 22(3):858–872

    PubMed  Google Scholar 

  27. Kumar S, Sharma SR (1998) Transmission of parasitic and competitor moulds of button mushroom through flies. Mushroom Research 7:25–28

    Google Scholar 

  28. Francisco J, Gea JC, Tello MJN (2010) Efficacy and effects on yield of different fungicides for control of wet bubble disease of mushroom caused by the mycoparasite Mycogone perniciosa. Crop Prot 29:1021–1025

    Google Scholar 

  29. Gandy DG, Spencer DM (1978) Fungicides for the control of Mycogone Perniciosa (Magn.), the cause of wet bubble on the cultivated mushroom. Sci Hortic 8:307–313

    CAS  Google Scholar 

  30. Garcha HS (1978) Diseases of mushroom and their control. Indian Mushroom Sci 1:185–191

    Google Scholar 

  31. Glamoalija J, Sokovia M, Vukojevia J, Milenkovia I, Griensven LJLDV (2006) Chemical composition and antifungal activities of essential oils of Satureja Thymbra L. and Salvia Pomifera sp. Calycina (sm.) Hayek. J Essent Oil Res 18:115–117

    Google Scholar 

  32. Singh M, Singh RP (2005) Management of mushroom pathogens through botanicals. Indian Phytopathol 58:189–193

    Google Scholar 

  33. Mishra SK, Singh RP (2003) Effect of biocides against Mycogone Perniciosa, a aycoparasite of Agaricus bisporus. Mushroom Res 12:105–112

    Google Scholar 

  34. Gandy DG (1979) Inhibition of Mycogone perniciosa growth by Acremonium strictum. Trans Br Mycol Soc 72:151–154

    Google Scholar 

  35. Li D, Sossah FL, Yang Y, Liu Z, Dai Y, Song B, Fu Y, Li Y (2019) Genetic and pathogenic variability of Mycogone perniciosa isolates causing wet bubble disease on Agaricus bisporus in China. Pathogens 8(4):179. https://doi.org/10.3390/pathogens8040179

    Article  CAS  PubMed Central  Google Scholar 

  36. Wang W, Li X, Chen B, Wang S, Li C, Wen Z (2016) Analysis of genetic diversity and development of scar markers in a Mycogone Perniciosa population. Curr Microbiol 73:9–14

    CAS  PubMed  Google Scholar 

  37. Kouser S, Ahmed M, Shah S (2013) Disease status and yield losses due to wet bubble disease (Mycogone perniciosa) associated with the cultivation of white button mushroom at different mushroom units of Kashmir Valley. Plant Pathol J 12(2):104–109

    Google Scholar 

  38. Li D, Sossah FL, Sun L, Fu Y, Li Y (2019) Genome analysis of Hypomyces perniciosus, the causal agent of wet bubble disease of button mushroom (Agaricus bisporus). Genes 10(6):417. https://doi.org/10.3390/genes10060417

    Article  CAS  PubMed Central  Google Scholar 

  39. Schmidt SM, Lukasiewicz J, Farrer R, Van Dam P, Bertoldo C, Rep M (2016) Comparative genomics of Fusarium oxysporum f. sp. melonis reveals the secreted protein recognized by the fom-2 resistance gene in melon. New Phytolgist 209:307–318

    CAS  Google Scholar 

  40. Banks AM, Farhana A, Katherine W, Thomas B, Gary LAB, Gary DF, Andy MB (2019) Genome sequence of Lecanicillium fungicola 150–1, the causal agent of dry bubble disease. Microbiol Resourc Announc 8(19):e00340-e419

    Google Scholar 

  41. Sossah F, Zhenghui L, Chentao Y, Benjamin O, Lei S, Yongping F, Yu L (2019) Genome sequencing of Cladobotryum protrusum provides insights into the evolution and pathogenic mechanisms of the cobweb disease pathogen on cultivated mushroom. Genes 10(2):e124

    PubMed  Google Scholar 

  42. Xu R, Xiaochen L, Bing P, Peibin L, Zhuang L, Yueting D, Shijun X (2020) Genomic features of Cladobotryum dendroides, which causes cobweb disease in edible mushrooms, and identification of genes related to pathogenicity and mycoparasitism. Pathogens 9(3):e232

    PubMed  Google Scholar 

  43. Pachauri S, Sherkhane PD, Kumar V, Mukherjee PK (2020) Whole genome sequencing reveals major deletions in the genome of M7, a gamma ray-induced mutant of Trichoderma virens that is repressed in conidiation, secondary metabolism, and mycoparasitism. Front Microbiol. https://doi.org/10.3389/fmicb.2020.01030

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Bankevich A, Nurk S, Antipov D (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32:309–312

    Google Scholar 

  47. Fang W, Latge JP (2018) Microbe Profile: Aspergillus fumigatus: a saprotrophic and opportunistic fungal pathogen. Microbiology 164:1009–1011

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12(1):59–60

    CAS  PubMed  Google Scholar 

  49. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  50. Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 12. https://doi.org/10.1155/2008/619832

  51. Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185

    Google Scholar 

  52. Nishimura O, Hara Y, Kuraku S (2017) gVolante for standardizing completeness assessment of genome and transcriptome assemblies. Bioinformatics 33(22):3635–3637

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067

    CAS  PubMed  Google Scholar 

  54. Kriventseva EV, Simao FA, Klioutchnikov G, Seppey M, Manni M, Ioannidis P, Waterhouse RM, Zdobnov EM (2017) BUSCO Applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol 35:543–554

    PubMed Central  Google Scholar 

  55. Wang Y, Coleman-Derr D, Chen G, Gu YQ (2015) OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 43(W1):W78-84

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Fan H, Ives A, Surget-Groba Y, Cannon C (2015) An assembly and alignment-free method of phylogeny reconstruction from next-generation sequencing data. BMC Genomics 16:522

    PubMed  PubMed Central  Google Scholar 

  57. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    CAS  PubMed  Google Scholar 

  58. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Winnenburg R, Baldwin TK, Urban M, Rawlings C, Kohler J, Hammond-Kosack KE (2006) PHI-base: a new database for pathogen host interactions. Nucleic Acids Res 34:459–464

    Google Scholar 

  60. Verma S, Gazara RK, Nizam S, Parween S, Chattopadhyay D, Verma PK (2016) Draft genome sequencing and secretome analysis of fungal phytopathogen Ascochyta rabiei provides insight into the necrotrophic effector repertoire. Sci Rep 6:24638

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40:26–32

    Google Scholar 

  62. Maria BC, Mejia SJ, Alberto E (2014) Efficiency of treatments for controlling Trichoderma spp during spawning in cultivation of lignicolous mushrooms. Braz J Microbiol 45(4):1263–1270

    Google Scholar 

  63. Yu C, Xin L (2020) Trichoderma koningiopsis controls Fusarium oxysporum causing damping-off in Pinus massoniana seedlings by regulating active oxygen metabolism, osmotic potential, and the rhizosphere microbiome. Bio Control 150. https://doi.org/10.1016/j.biocontrol.2020.104352

  64. Karlsson M, Atanasova L, Jensen DF, Zeilinger S (2017) Necrotrophic mycoparasites and their genomes. Microbiol Spectr 5. https://doi.org/10.1128/microbiolspec.FUNK-0016-2016

  65. Dodds PN, Rafiqi M, Gan PHP, Hardham AR, Jones DA, Ellis JG (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol 183:993–1000

    PubMed  Google Scholar 

  66. Levin E, Kishore A, Ballester AR, Raphael G, Feigenberg O, Liu Y, Norelli J, Gonzalez-Candelas L, Wisniewski M, Droby S (2019) Identification of pathogenicity-related genes and the role of a subtilisin-related peptidase S8 (PePRT) in authophagy and virulence of Penicillium expansum on apples. Postharvest Biol Technol 149:209–220

    CAS  Google Scholar 

  67. Kombrink A, Thomma BPHJ (2013) LysM effectors: secreted proteins supporting fungal life. PLoS Pathog 9(12):e1003769. https://doi.org/10.1371/journal.ppat.1003769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Garcia Rubio R, Oliveira HCD, Rivera J, Trevijano Contador N (2020) The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02993

    Article  PubMed  PubMed Central  Google Scholar 

  69. Novaes-Ledieu M, Mendoza CG (1981) The cell walls of Agaricus bisporus and Agaricus campestris fruiting body hyphae. Can J Microbiol 27(8):779–787

    CAS  PubMed  Google Scholar 

  70. Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    CAS  PubMed  Google Scholar 

  71. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 22:43–56

    Google Scholar 

  73. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    CAS  PubMed  Google Scholar 

  74. Hunsley D, Bumett JH (1970) The ultra-structural architecture of the walls of some hyphal fungi. J Gen Microbiol 62:203–218

    CAS  Google Scholar 

  75. Ridout CJ, Coley-Smith JR, Lynch JM (1988) Fractionation of extracellular enzymes from a mycoparasitic strain of Trichoderma harzianum. Enzyme Microb Technol 10:180–187

    CAS  Google Scholar 

Download references

Funding

This work is funded by the ICAR- Directorate of Mushroom Research, Chambaghat, Solan, Himachal Pradesh, 173213 under an institutional project.

Author information

Authors and Affiliations

Authors

Contributions

Material preparation, data collection, and analysis and preparation of the first draft were performed by Anil Kumar. All the co-authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Anil Kumar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Derlene Attili Agellis

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, A., Sharma, V.P., Kumar, S. et al. De novo genome sequencing of mycoparasite Mycogone perniciosa strain MgR1 sheds new light on its biological complexity. Braz J Microbiol 52, 1545–1556 (2021). https://doi.org/10.1007/s42770-021-00535-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-021-00535-x

Keywords

Navigation