1887

Microbiology Society logo

Volume 165, Issue 6

Casing microbiome dynamics during button mushroom cultivation: implications for dry and wet bubble diseases Open Access

Abstract

The casing material required in mushroom cultivation presents a very rich ecological niche, which is inhabited by a diverse population of bacteria and fungi. In this work three different casing materials, blonde peat, black peat and a 50 : 50 mixture of both, were compared for their capacity to show a natural suppressive response against dry bubble, Lecanicillium fungicola (Preuss) Zare and Gams, and wet bubble, Mycogone perniciosa (Magnus) Delacroix. The highest mushroom production was collected from crops cultivated using the mixed casing and black peat, which were not significantly different in yield. However, artificial infection with mycoparasites resulted in similar yield losses irrespective of the material used, indicating that the casing materials do not confer advantages in disease suppression. The composition of the microbiome of the 50 : 50 casing mixture along the crop cycle and the compost and basidiomes was evaluated through next-generation sequencing (NGS) of the V3–V4 region of the bacterial 16S rRNA gene and the fungal ITS2 region. Once colonized by Agaricus bisporus, the bacterial diversity of the casing microbiome increased and the fungal diversity drastically decreased. From then on, the composition of the casing microbiome remained relatively stable. Analysis of the composition of the bacterial microbiome in basidiomes indicated that it is highly influenced by the casing microbiota. Notably, L. fungicola was consistently detected in uninoculated control samples of compost and casing using NGS, even in asymptomatic crops. This suggests that the naturally established casing microbiota was able to help to suppress disease development when inoculum levels were low, but was not effective in suppressing high pressure from artificially introduced fungal inoculum. Determination of the composition of the casing microbiome paves the way for the development of synthetic casing communities that can be used to investigate the role of specific components of the casing microbiota in mushroom production and disease control.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Agaricus bisporus , casing material , metagenomics , microbiome , mycoparasites and next generation sequencing
© 2019 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000792
2019-04-17
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/165/6/611.html?itemId=/content/journal/micro/10.1099/mic.0.000792&mimeType=html&fmt=ahah

References

  1. Reis FS, Barros L, Martins A, Ferreira IC. Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: an inter-species comparative study. Food Chem Toxicol 2012; 50:191–197 [View Article][PubMed]
     [Google Scholar]
  2. Royse DJ, Baars J, Tan Q. Current overview of mushroom production in the world. In Zied DC, Pardo-Giménez A. (editors) Edible and Medicinal Mushrooms: Technology and Applications Hoboken, NJ, USA: John Wiley and Sons Ltd; 2017 pp. 5–13
     [Google Scholar]
  3. Kertesz MA, Thai M. Compost bacteria and fungi that influence growth and development of Agaricus bisporus and other commercial mushrooms. Appl Microbiol Biotechnol 2018; 102:1639–1650 [View Article][PubMed]
     [Google Scholar]
  4. Pardo A, Emilio Pardo J, de Juan JA, Zied DC. Modelling the effect of the physical and chemical characteristics of the materials used as casing layers on the production parameters of Agaricus bisporus. Arch Microbiol 2010; 192:1023–1030 [View Article][PubMed]
     [Google Scholar]
  5. Zarenejad F, Yakhchali B, Rasooli I. Evaluation of indigenous potent mushroom growth promoting bacteria (MGPB) on Agaricus bisporus production. World J Microbiol Biotechnol 2012; 28:99–104 [View Article][PubMed]
     [Google Scholar]
  6. Colauto NB, Fermor TR, Eira AF, Linde GA. Pseudomonas putida Stimulates Primordia on Agaricus bitorquis. Curr Microbiol 2016; 72:482–488 [View Article][PubMed]
     [Google Scholar]
  7. Siyoum NA, Surridge K, van der Linde EJ, Korsten L. Microbial succession in white button mushroom production systems from compost and casing to a marketable packed product. Ann Microbiol 2016; 66:151–164 [View Article]
     [Google Scholar]
  8. Berendsen RL, Kalkhove SI, Lugones LG, Wösten HA, Bakker PA. Germination of Lecanicillium fungicola in the mycosphere of Agaricus bisporus. Environ Microbiol Rep 2012; 4:227–233 [View Article][PubMed]
     [Google Scholar]
  9. Largeteau ML, Savoie JM. Microbially induced diseases of Agaricus bisporus: biochemical mechanisms and impact on commercial mushroom production. Appl Microbiol Biotechnol 2010; 86:63–73 [View Article][PubMed]
     [Google Scholar]
  10. Gea FJ, Tello JC, Navarro M-J. Efficacy and effects on yield of different fungicides for control of wet bubble disease of mushroom caused by the mycoparasite Mycogone perniciosa. Crop Prot 2010; 29:1021–1025 [View Article]
     [Google Scholar]
  11. Berendsen RL, Baars JJ, Kalkhove SI, Lugones LG, Wösten HA et al. Lecanicillium fungicola: causal agent of dry bubble disease in white-button mushroom. Mol Plant Pathol 2010; 11:585–595 [View Article][PubMed]
     [Google Scholar]
  12. McGee CF, Byrne H, Irvine A, Wilson J. Diversity and dynamics of the DNA and cDNA-derived bacterial compost communities throughout the Agaricus bisporus mushroom cropping process. Ann Microbiol 2017; 67:751–761 [View Article]
     [Google Scholar]
  13. McGee CF, Byrne H, Irvine A, Wilson J. Diversity and dynamics of the DNA- and cDNA-derived compost fungal communities throughout the commercial cultivation process for Agaricus bisporus. Mycologia 2017; 109:475–484 [View Article][PubMed]
     [Google Scholar]
  14. Vieira FR, Pecchia JA. An Exploration into the Bacterial Community under Different Pasteurization Conditions during Substrate Preparation (Composting-Phase II) for Agaricus bisporus Cultivation. Microb Ecol 2018; 75:318–330 [View Article][PubMed]
     [Google Scholar]
  15. Cai W-M, Yao H-Y, Feng W-L, Jin Q-L, Liu Y-Y et al. Microbial Community Structure of Casing Soil During Mushroom Growth. Pedosphere 2009; 19:446–452 [View Article]
     [Google Scholar]
  16. Choudhary DK. First Preliminary Report on Isolation and Characterization of Novel Acinetobacter spp. in Casing Soil Used for Cultivation of Button Mushroom, Agaricus bisporus (Lange) Imbach. Int J Microbiol 2011; 2011:1–6 [View Article][PubMed]
     [Google Scholar]
  17. Jurak E, Patyshakuliyeva A, de Vries RP, Gruppen H, Kabel MA. Compost Grown Agaricus bisporus Lacks the Ability to Degrade and Consume Highly Substituted Xylan Fragments. PLoS One 2015; 10:e0134169 [View Article][PubMed]
     [Google Scholar]
  18. Kabel MA, Jurak E, Mäkelä MR, de Vries RP. Occurrence and function of enzymes for lignocellulose degradation in commercial Agaricus bisporus cultivation. Appl Microbiol Biotechnol 2017; 101:4363–4369 [View Article][PubMed]
     [Google Scholar]
  19. Wang L, Mao J, Zhao H, Li M, Wei Q et al. Comparison of characterization and microbial communities in rice straw- and wheat straw-based compost for Agaricus bisporus production. J Ind Microbiol Biotechnol 2016; 43:1249–1260 [View Article][PubMed]
     [Google Scholar]
  20. Vos AM, Heijboer A, Boschker HTS, Bonnet B, Lugones LG et al. Microbial biomass in compost during colonization of Agaricus bisporus. AMB Express 2017; 7:12 [View Article][PubMed]
     [Google Scholar]
  21. Székely AJ, Sipos R, Berta B, Vajna B, Hajdú C et al. DGGE and T-RFLP analysis of bacterial succession during mushroom compost production and sequence-aided T-RFLP profile of mature compost. Microb Ecol 2009; 57:522–533 [View Article][PubMed]
     [Google Scholar]
  22. Kertesz M, Safianowicz K, Bell T. New insights into the microbial communities and biological activities that define mushroom compost. In Baars JJP, Sonnenberg ASM. (editors) Proceedings of the 19th International Congress on the Science and Cultivation of Edible and Medicinal Fungi Amsterdam, The Netherlands: 2016 pp. 161–165
     [Google Scholar]
  23. Sébastien M S, Martinez-Medina M, Jijakli MH. Biological control in the microbiome era: challenges and opportunities. Biol Control 2015; 89:98–108
     [Google Scholar]
  24. Carrasco J, Navarro MJ, Santos M, Diánez F, Gea FJ. Incidence, identification and pathogenicity of Cladobotryum mycophilum , causal agent of cobweb disease on Agaricus bisporus mushroom crops in Spain. Ann Appl Biol 2016; 168:214–224 [View Article]
     [Google Scholar]
  25. Pardo-Giménez A, Catalán L, Carrasco J, Álvarez-Ortí M, Zied D et al. Effect of supplementing crop substrate with defatted pistachio meal on Agaricus bisporus and Pleurotus ostreatus production. J Sci Food Agric 2016; 96:3838–3845 [View Article][PubMed]
     [Google Scholar]
  26. Rocchi S, Valot B, Reboux G, Millon L. DNA metabarcoding to assess indoor fungal communities: Electrostatic dust collectors and Illumina sequencing. J Microbiol Methods 2017; 139:107–112 [View Article][PubMed]
     [Google Scholar]
  27. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 2013; 41:e1 [View Article][PubMed]
     [Google Scholar]
  28. White T, Bruns T, Lee S. Taylor J amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis M, Gelfand D, Shinsky J, White T. (editors) PCR Protocols: a Guide to Methods and Applications San Diego: Academic Press; 1990 pp. 315–322
     [Google Scholar]
  29. Andrews S. FastQC: a quality control tool for high throughput sequence dataAvailable online at; 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  30. Krueger F. Trim Galore!: A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files; 2015 http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/
  31. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335–336 [View Article][PubMed]
     [Google Scholar]
  32. Desantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72:5069–5072 [View Article][PubMed]
     [Google Scholar]
  33. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 2013; 22:5271–5277 [View Article][PubMed]
     [Google Scholar]
  34. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
     [Google Scholar]
  35. Dhariwal A, Chong J, Habib S, King IL, Agellon LB et al. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 2017; 45:W180–W188 [View Article][PubMed]
     [Google Scholar]
  36. Wang Y, Xu L, Gu YQ, Coleman-Derr D. MetaCoMET: a web platform for discovery and visualization of the core microbiome. Bioinformatics 2016; 32:btw507–3470 [View Article][PubMed]
     [Google Scholar]
  37. Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 2011; 12:385 [View Article][PubMed]
     [Google Scholar]
  38. Pardo A, de Juan AJ, Pardo J. Assessment of different casing materials for use as peat alternatives in mushroom cultivation. Evaluation of quantitative and qualitative production parameters. Spanish Journal of Agricultural Research 2004; 2:267–272 [View Article]
     [Google Scholar]
  39. Bacaro G, Altobelli A, Cameletti M, Ciccarelli D, Martellos S et al. Incorporating spatial autocorrelation in rarefaction methods: Implications for ecologists and conservation biologists. Ecol Indic 2016; 69:233–238 [View Article]
     [Google Scholar]
  40. Zare R, Gams W. A revision of the Verticillium fungicola species complex and its affinity with the genus Lecanicillium. Mycol Res 2008; 112:811–824 [View Article][PubMed]
     [Google Scholar]
  41. Kumar N, Mishra AB, Bharadwaj MC. Effect of Verticillium fungicola (Preuss) hassebr inoculation in casing soil and conidial spray on white button mushroom Agaricus bisporous. Afr J Agric Res 2014; 9:1141–1143
     [Google Scholar]
  42. Kanchiswamy CN, Malnoy M, Maffei ME. Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci 2015; 20:206–211 [View Article][PubMed]
     [Google Scholar]
  43. Kües U, Khonsuntia W, Subba S, Dörnte B. Volatiles in communication of Agaricomycetes. In Schüfflerpp AT. (editor) Physiology and Genetics Springer, Cham: 2018 pp. 149–212
     [Google Scholar]
  44. Berendsen RL, Kalkhove SI, Lugones LG, Baars JJ, Wösten HA et al. Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease. Appl Microbiol Biotechnol 2013; 97:5535–5543 [View Article][PubMed]
     [Google Scholar]
  45. Piasecka J, Kavanagh K, Grogan H. Detection of sources of Lecanicillium (Verticillium) fungicola on mushroom farms. In Savoie JM, Foulongne-Oriol M, Largeteau M, Barroso G. (editors) Proceedings of the 7th International Conference on Mushroom Biology and Mushroom Products Arcachon, France: 2011 pp. 479–484
     [Google Scholar]
  46. Tibbles LL, Chandler D, Mead A, Jervis M, Boddy L. Evaluation of the behavioural response of the flies Megaselia halterata and Lycoriella castanescens to different mushroom cultivation materials. Entomol Exp Appl 2005; 116:73–81 [View Article]
     [Google Scholar]
  47. Thomas P, Sekhar AC. Effects due to rhizospheric soil application of an antagonistic bacterial endophyte on native bacterial community and its survival in soil: a case study with Pseudomonas aeruginosa from Banana. Front Microbiol 2016; 7:493 [View Article][PubMed]
     [Google Scholar]
  48. Leveau JH, Preston GM. Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol 2008; 177:859–876 [View Article][PubMed]
     [Google Scholar]
  49. Noble R, Dobrovin-Pennington A, Hobbs PJ, Pederby J, Rodger A. Volatile C8 compounds and pseudomonads influence primordium formation of Agaricus bisporus. Mycologia 2009; 101:583–591 [View Article][PubMed]
     [Google Scholar]
  50. Rainey PB. Effect of Pseudomonas putida on hyphal growth of Agaricus bisporus. Mycol Res 1991; 95:699–704 [View Article]
     [Google Scholar]
  51. Zhang C, Huang T, Shen C, Wang X, Qi Y et al. Downregulation of ethylene production increases mycelial growth and primordia formation in the button culinary-medicinal mushroom, Agaricus bisporus (Agaricomycetes). Int J Med Mushrooms 2016; 18:1131–1140 [View Article][PubMed]
     [Google Scholar]
  52. Doores S, Kramer M, Beelman R. Evaluation and bacterial populations associated with fresh mushrooms (Agaricus bisporus). In Wuest PJ, Royse DJ, Beelman RB. (editors) Cultivating edible fungi Elsevier; 1987 pp. 283–294
     [Google Scholar]
  53. Royse DJ, Sanchez JE, Beelman RB, Davidson J. Re-supplementing and re-casing mushroom (Agaricus bisporus) compost for a second crop. World Journal of Microbiology and Biotechnology 2008; 24:319–325 [View Article]
     [Google Scholar]
  54. Berendsen RL, Kalkhove SIC, Lugones LG, Baars JJP, Wösten HAB et al. Effects of fluorescent Pseudomonas spp. isolated from mushroom cultures on Lecanicillium fungicola. Biological Control 2012; 63:210–221 [View Article]
     [Google Scholar]
  55. Kadouri D, O'Toole GA. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 2005; 71:4044–4051 [View Article][PubMed]
     [Google Scholar]
  56. Harini K, Ajila V, Hegde S. Bdellovibrio bacteriovorus: a future antimicrobial agent?. J Indian Soc Periodontol 2013; 17:823–825 [View Article][PubMed]
     [Google Scholar]
  57. Saxon EB, Jackson RW, Bhumbra S, Smith T, Sockett RE. Bdellovibrio bacteriovorus HD100 guards against Pseudomonas tolaasii brown-blotch lesions on the surface of post-harvest Agaricus bisporus supermarket mushrooms. BMC Microbiol 2014; 14:163 [View Article][PubMed]
     [Google Scholar]
  58. McGee CF. Microbial ecology of the Agaricus bisporus mushroom cropping process. Appl Microbiol Biotechnol 2018; 102:1075–1083 [View Article][PubMed]
     [Google Scholar]
  59. Pecchia J, Cortese R, Albert I. Investigation into the microbial community changes that occur in the casing layer during cropping of the white button mushroom, Agaricus bisporus. In Singh M. (editor) Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products New Delhi, India: 2014 pp. 309–313
     [Google Scholar]
  60. Safianowicz K, Bell TL, Kertesz MA. Bacterial population dynamics in recycled mushroom compost leachate. Appl Microbiol Biotechnol 2018; 102:5335–5342 [View Article][PubMed]
     [Google Scholar]
  61. Badotti F, de Oliveira FS, Garcia CF, Vaz AB, Fonseca PL et al. Effectiveness of ITS and sub-regions as DNA barcode markers for the identification of Basidiomycota (Fungi). BMC Microbiol 2017; 17:42 [View Article][PubMed]
     [Google Scholar]
  62. Carrasco J, Navarro M-J, Gea FJ. Cobweb, a serious pathology in mushroom crops: A review. Spanish Journal of Agricultural Research 2017; 15:e10R01 [View Article]
     [Google Scholar]
  63. Zhang C, Kakishima M, Xu J, Wang Q, Li Y. The effect of Hypomyces perniciosus on the mycelia and basidiomes of Agaricus bisporus. Microbiology 2017; 163:1273–1282 [View Article][PubMed]
     [Google Scholar]
  64. Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 2002; 40: [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000792
Loading
Casing microbiome dynamics during button mushroom cultivation: implications for dry and wet bubble diseases
Microbiology 165, 611 (2019); https://doi.org/10.1099/mic.0.000792
/content/journal/micro/10.1099/mic.0.000792
/content/journal/micro/10.1099/mic.0.000792
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error