Abstract
Mushrooms are an important food crop throughout the world. The most important edible mushroom is the button mushroom (Agaricus bisporus), which comprises about 30% of the global mushroom market. This species is cultivated commercially on a selective compost that is produced predominantly from wheat straw/stable bedding and chicken manure, at a moisture content of around 70% (w/w) and temperatures of up to 80 °C. Large volumes of water are required to achieve this moisture content, and many producers therefore collect leachate from the composting windrows and bunkers (known in the industry as “goody water”) and reuse it to wet the raw ingredients. This has the benefit of recycling and saving water and has the potential to enrich beneficial microorganisms that stimulate composting, but also the risk of enhancing pathogen populations that could reduce productivity. Here, we show by 16S rRNA gene sequencing that mushroom compost leachate contains a high diversity of unknown microbes, with most of the species found affiliated with the phyla Firmicutes and Proteobacteria. However, by far the most abundant species was the thermophile Thermus thermophilus, which made up approximately 50% of the bacterial population present. Although the leachate was routinely collected and stored in an aerated central storage tank, many of the bacterial species found in leachate were facultative anaerobes. However, there was no evidence for sulfide production, and no sulfate-reducing bacterial species were detected. Because T. thermophilus is important in the high temperature phase of composting, the use of recycled leachate as an inoculum for the raw materials is likely to be beneficial for the composting process.
Similar content being viewed by others
References
Arrigo N, Holderegger R, Alvarez N (2012) Automated scoring of AFLPs using RawGeno v 2.0, a free R CRAN library. Meth Molec Biol 888:155–175. https://doi.org/10.1007/978-1-61779-870-2_10
Beffa T, Blanc M, Lyon PF, Vogt G, Marchiani M, Fischer JL, Aragno M (1996) Isolation of Thermus strains from hot composts (60 to 80 °C). Appl Environ Microbiol 62:1723–1727
Bergquist PL, Gibbs MD, Morris DD, Te'o VS, Saul DJ, Moran HW (1999) Molecular diversity of thermophilic cellulolytic and hemicellulolytic bacteria. FEMS Microbiol Ecol 28:99–110. https://doi.org/10.1111/j.1574-6941.1999.tb00565.x
Blanc M, Marilley L, Beffa T, Aragno M (1999) Thermophilic bacterial communities in hot composts as revealed by most probable number counts and molecular (16S rDNA) methods. FEMS Microbiol Ecol 28:141–149. https://doi.org/10.1111/j.1574-6941.1999.tb00569.x
Bolan NS, Szogi AA, Chuasavathi T, Seshadri B, Rothrock MJ, Panneerselvam P (2010) Uses and management of poultry litter. Worlds Poult Sci J 66:673–698. https://doi.org/10.1017/s0043933910000656
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
Chang S-T, Miles PG (2004) Mushrooms: cultivation, nutritional value, medicinal effect and environmental impact, 2nd edn. CRC Press, Boca Raton
Charif D, Lobry JR (2007) Seqin{R} 1.0-2: a contributed package to the {R} project for statistical computing devoted to biological sequences retrieval and analysis. In: Bastolla U, Porto M, Roman HE, Vendruscolo M (eds) Structural approaches to sequence evolution: Molecules, networks, populations. Springer, New York, pp 207–232
Collado L, Figueras MJ (2011) Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 24:174–192. https://doi.org/10.1128/cmr.00034-10
Constantine W, Hesterberg T, Wittkowski K, Song T, Kaluzny S (2016) Supplemental S-PLUS functionality in R. R package version 1.2–2. R Foundation for Statistical Computing, Vienna, Austria. https://CRAN.R-project.org/package=splus2R Accessed 1 Nov 2017
Guo MX (2005) Groundwater quality under the influence of spent mushroom substrate weathering. J Environ Monit 7:1007–1012. https://doi.org/10.1039/b505522a
Henne A, Bruggemann H, Raasch C, Wiezer A, Hartsch T, Liesegang H, Johann A, Lienard T, Gohl O, Martinez-Arias R, Jacobi C, Starkuviene V, Schlenczeck S, Dencker S, Huber R, Klenk HP, Kramer W, Merkl R, Gottschalk G, Fritz HJ (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat Biotechnol 22:547–553. https://doi.org/10.1038/nbt956
Jurak E, Punt AM, Arts W, Kabel MA, Gruppen H (2015) Fate of carbohydrates and lignin during composting and mycelium growth of Agaricus bisporus on wheat straw based compost. PLoS One 10:e0138909. https://doi.org/10.1371/journal.pone.0138909
Kaplan LA, Standley LJ, Newbold JD (1995) Impact on water quality of high and low density applications of spent mushroom substrate to agricultural lands. Compost Sci Util 3:55–63. https://doi.org/10.1080/1065657x.1995.10701769
Kertesz M, Safianowicz K, Bell T (2016) New insights into the microbial communities and biological activities that define mushroom compost. Sci Cult Edible Fungi 19:161–165
Kertesz MA, Thai M (2018) Compost bacteria and fungi that influence growth and development of Agaricus bisporus and other commercial mushrooms. Appl Microbiol Biotechnol 102:1639–1650. https://doi.org/10.1007/s00253-018-8777-z
Li X (2005) PROcess: Ciphergen SELDI-TOF processing. R package version 1.54.0. R Foundation for Statistical Computing, Vienna, Austria. https://rdrr.io/bioc/PROcess/. Accessed 1 Nov 2017
Lyon PF, Beffa T, Blanc M, Auling G, Aragno M (2000) Isolation and characterization of highly thermophilic xylanolytic Thermus thermophilus strains from hot composts. Can J Microbiol 46:1029–1035. https://doi.org/10.1139/cjm-46-11-1029
Lyons G, Kilpatrick M, Sharma HSS, Noble R, Dobrovin-Pennington A, Hobbs P, Andrews F, Carmichael E (2008) Characterization of recycled mushroom compost leachate by chemical analysis and thermogravimetry-mass spectrometry. J Agric Food Chem 56:6488–6497. https://doi.org/10.1021/jf800487e
McGee CF, Byrne H, Irvine A, Wilson J (2017) Diversity and dynamics of the DNA and cDNA-derived bacterial compost communities throughout the Agaricus bisporus mushroom cropping process. Ann Microbiol 67:751–761. https://doi.org/10.1007/s13213-017-1303-1
Noble R (2006) Improving the efficiency and environmental impact of mushroom composting. Final Report, M 3e HortLINK Project CSA6365/HL0163LMU. Warwick HRI, Warwick
Noble R, Dobrovin-Pennington A, Wright C, Hobbs PJ, Williams J (2009) Aerating recycled water on mushroom composting sites affects its chemical analysis and the characteristics of odor emissions. J Environ Qual 38:1493–1500. https://doi.org/10.2134/jeq2008.0145
Noble R, Hobbs PJ, Dobrovin-Pennington A, Misselbrook TH, Mead A (2001) Olfactory response to mushroom composting emissions as a function of chemical concentration. J Environ Qual 30:760–767
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2016) vegan: Community ecology package in R. R package version 2.3-4. R Foundation for Statistical Computing, Vienna, Austria. https://CRAN.R-project.org/package=vegan. Accessed 1 Nov 2017
Perttula M, Ratto M, Kondradsdottir M, Kristjansson JK, Viikari L (1993) Xylanases of thermophilic bacteria from Icelandic hot springs. Appl Microbiol Biotechnol 38:592–595
R Core team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 1 Nov 2017
Racine JS (2012) RStudio: a platform-independent IDE for R and Sweave. J Appl Econ 27:167–172. https://doi.org/10.1002/jae.1278
Regueiro L, Carballa M, Lema JM (2014) Outlining microbial community dynamics during temperature drop and subsequent recovery period in anaerobic co-digestion systems. J Biotechnol 192:179–186. https://doi.org/10.1016/j.jbiotec.2014.10.007
Rothrock MJ, Cook KL, Warren JG, Eiteman MA, Sistani K (2010) Microbial mineralization of organic nitrogen forms in poultry litters. J Environ Qual 39:1848–1857. https://doi.org/10.2134/jeq2010.0024
Royse DJ (2014) A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia and Flammulina. In: Singh M (ed) Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products. New Delhi, pp 1–6
Ryckeboer J, Mergaert J, Vaes K, Klammer S, De Clercq D, Coosemans J, Insam H, Swings J (2003) A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol 53:349–410
Szekely A, Sipos R, Berta B, Vajna B, Hajdu C, Marialigeti K (2009) DGGE and T-RFLP analysis of bacterial succession during mushroom compost production and sequence-aided T-RFLP profile of mature compost. Microb Ecol 57:522–533. https://doi.org/10.1007/s00248-008-9424-5
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Winsley T, van Dorst JM, Brown MV, Ferrari BC (2012) Capturing greater 16S rRNA gene sequence diversity within the domain Bacteria. Appl Environ Microbiol 78:5938–5941. https://doi.org/10.1128/aem.01299-12
Wu YW, Joshua C, Eichorst SA, Gladden JM, Simmons BA, Singer SW (2015) Genomic analysis of xylose metabolism in members of the Deinoccocus-Thermus phylum from thermophilic biomass-deconstructing bacterial consortia. BioEnergy Res 8:1031–1038. https://doi.org/10.1007/s12155-015-9600-7
Xie Y (2013) knitr: a general purpose package for dynamic report generation in R. R Package version 1.20. R Foundation for Statistical Computing, Vienna, Austria. https://CRAN.R-project.org/package=knitr. Accessed 1 Nov 2017
Acknowledgements
We thank our industry partners, especially ELF Farm Supplies in Mulgrave, NSW, Australia, for their kind assistance with sampling and processing, and for their helpful advice on many aspects of mushroom composting.
Funding
This work was supported by grant MU10021 from Horticulture Innovation Australia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Supplemental Table S1
(XLSX 83 kb)
Rights and permissions
About this article
Cite this article
Safianowicz, K., Bell, T.L. & Kertesz, M.A. Bacterial population dynamics in recycled mushroom compost leachate. Appl Microbiol Biotechnol 102, 5335–5342 (2018). https://doi.org/10.1007/s00253-018-9007-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9007-4