Abstract
Fungi capable of producing fruit bodies are essential food and medicine resources. Despite recent advances in the study of microbial communities in mycorrhizospheres, little is known about the bacterial communities contained in fruit bodies. Using high-throughput sequencing, we investigated the bacterial communities in four species of mushrooms located on the alpine meadow and saline-alkali soil of the Qinghai-Tibet Plateau (QTP). Proteobacteria (51.7% on average) and Actinobacteria (28.2% on average) were the dominant phyla in all of the sampled fairy ring fruit bodies, and Acidobacteria (27.5% on average) and Proteobacteria (25.7% on average) dominated their adjacent soils. For the Agria. Bitorquis, Actinobacteria was the dominant phylum in its fruit body (67.5% on average) and adjacent soils (65.9% on average). The alpha diversity (i.e., Chao1, Shannon, Richness, and Simpson indexes) of the bacterial communities in the fruit bodies were significantly lower than those in the soil samples. All of the fungi shared more than half of their bacterial phyla and 16.2% of their total operational taxonomic units (OTUs) with their adjacent soil. Moreover, NH4+ and pH were the key factors associated with bacterial communities in the fruit bodies and soils, respectively. These results indicate that the fungi tend to create a unique niche that selects for specific members of the bacterial community. Using culture-dependent methods, we also isolated 27 bacterial species belonging to three phyla and five classes from fruit bodies and soils. The strains isolated will be useful for future research on interactions between mushroom-forming fungi and their bacterial endosymbionts.
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Data Availability
Sequence files for all samples used in this study have been deposited at NCBI with accession: MK910221–MK910224, MK920120–MK920145, and MK963008.
References
Antonybabu S, Deveau A, Van Nostrand JD et al (2014) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16:2831–2847. https://doi.org/10.1111/1462-2920.12294
Barbieri E, Ceccaroli P, Saltarelli R et al (2010) New evidence for nitrogen fixation within the Italian white truffle Tuber magnatum. Fungal Biologe 114:936–942
Benucci G, Bonito GM (2016) The truffle microbiome: species and geography effects on bacteria associated with fruiting bodies of hypogeous pezizales. Microb Ecol 72:4–8. https://doi.org/10.1007/s00248-016-0755-3
Boersma FGH, Otten R, Warmink JA, Nazir R, Elsas JDV (2010) Selection of Variovorax paradoxus-like bacteria in the mycosphere and the role of fungal-released compounds. Soil Biol Biochem 42:2137–2145. https://doi.org/10.1016/j.soilbio.2010.08.009
Bratek Z, Merényi Z, Illyés Z et al (2010) Studies on the ecophysiology of Tuber aestivum populations in the Carpatho-Pannonian region. Österreichische Zeitschrift Für Pilzkunde 10:221–226
Brinkman BM, Hildebrand F, Kubica M et al (2011) Caspase deficiency alters the murine gut microbiome. Cell Death Dis. https://doi.org/10.1038/cddis.2011.101
Burke DJ, Dunham SM, Kretzer AM (2010) Molecular analysis of bacterial communities associated with the roots of Douglas fir (Pseudotsuga menziesii) colonized by different ectomycorrhizal fungi. FEMS Microbiol Ecol 65:299–309. https://doi.org/10.1111/j.1574-6941.2008.00491.x
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carrasco J, Preston GM (2020) Growing edible mushrooms: a conversation between bacteria and fungi. Environ Microbiol 22:858–872. https://doi.org/10.1111/1462-2920.14765
Chong J, Liu P, Zhou G, Xia J (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc. https://doi.org/10.1038/s41596-019-0264-11-23
Chu H, Sun H, Tripathi BM, Adams JM, Huang R, Zhang Y, Shi Y (2016) Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau. Environ Microbiol 18:1523–1533. https://doi.org/10.1111/1462-2920.13236
Cullings K, Stott MB, Marinkovich N, DeSimone J, Bhardwaj S (2020) Phylum-level diversity of the microbiome of the extremophilic basidiomycete fungus Pisolithus arhizus (Scop.) Rauschert: an island of biodiversity in a thermal soil desert. Microbiol Open https://doi.org/10.1002/mbo3.1062
Daniyal G (2022) Global diversity and distribution of mushroom-inhabiting bacteria. Environ Microbiol Rep 14:254–264. https://doi.org/10.1111/1758-2229.13045
De L, Laura DB, Cristina DM, Navarro-Noya YE, Marco LG, Luc D (2017) Reducing salinity by flooding an extremely alkaline and saline soil changes the bacterial community but its effect on the archaeal community is limited. Front Microbiol. https://doi.org/10.3389/fmicb.2017.0046
Deveau A, Palin B, Delaruelle C et al (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755. https://doi.org/10.1111/j.1469-8137.2007.02148.x
Deveau A, Antony-Babu S, Tacon FL, Robin C, Frey-Klett P, Uroz S (2016) Temporal changes of bacterial communities in the Tuber melanosporum ectomycorrhizosphere during ascocarp development. Mycorrhiza 26:389–399. https://doi.org/10.1007/s00572-015-0679-7
Deveau A, Labbe J (2016) Mycorrhiza helper bacteria. John Wiley and Sons Inc.,Hoboken,New Jersey, United States of America, United States. https://doi.org/10.1002/9781118951446.ch24
Edgar RCJB (2010) Search and clustering orders of magnitude faster than BLAST. 26:2460-2461.https://doi.org/10.1093/bioinformatics/btq461
Fox RTV (2006) Fungal foes in your garden: fairy ring mushrooms. Mycologist 20:36–37. https://doi.org/10.1016/j.mycol.2005.11.013
Frey-Klett P, Garbaye J, Tarkka MT (2007) Tansley Review: The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
Garbaye J, Churin JL, Duponnois R (1992) Effects of substrate sterilization, fungicide treatment, and mycorrhization helper bacteria on ectomycorrhizal formation of pedunculate oak ( Quercus robur ) inoculated with Laccaria laccata in two peat bare-root nurseries. Biol Fertil Soils 13:55–57. https://doi.org/10.1007/BF00337239
García-Montero LG, Casermeiro MA, Hernando I, Hernando J (2007) Effect of active carbonate, exchangeable calcium, and stoniness of soil on Tuber melanosporum carpophore production. New Zealand J Crop Hortic Sci 35:139–146. https://doi.org/10.1080/01140670709510178
García-Montero L, Casermeiro MA, Hernando J, Hernando IJAJoSR (2006) Soil factors that influence the fruiting of Tuber melanosporum (black truffle). 44:731-738.https://doi.org/10.1071/SR06046
Gohar D, Pent M, Pldmaa K, Bahram M (2020) Bacterial community dynamics across developmental stages of fungal fruiting bodies. FEMS Microbiol Ecol 96:https://doi.org/10.1093/femsec/fiaa1175
Guillaume Bertault FR, Fernandez D, Berthomieu A, Hochberg ME, Callot G, Raymond M (2001) Population genetics and dynamics of the black truffle in a man-made truffle field. Heredity 86:451–458. https://doi.org/10.1046/J.1365-2540.2001.00855.X
Herlemann DPR, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Hong-Yan Bai A-YZ, Mei Y, Man Xu, Xiao-Lin Lu, Dai C-C, Jia Y (2021) Effects of ectomycorrhizal fungus bolete identity on the community assemblages of endofungal bacteria. Environ Microbiol Rep 13:852–861. https://doi.org/10.1111/1758-2229.13007
Kumar S, Tamura K, Jakobsen IB, Nei M (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. https://doi.org/10.1093/molbev/msm092
Labbé JL, Weston DJ, Dunkirk N, Pelletier DA, Tuskan GA (2014) Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. Front Plant Sci 510.3389/fpls.2014.00579
Lewis WH, Tahon G, Geesink P, Sousa DZ, Ettema T (2020) Innovations to culturing the uncultured microbial majority. Nat Rev Microbiol 19:225–240. https://doi.org/10.1038/s41580-021-00383-5
Li Q, Li X, Chen C, Li S, Zheng L (2016) Analysis of bacterial diversity and communities associated with Tricholoma matsutake fruiting bodies by barcoded pyrosequencing in Sichuan Province, Southwest China. J Microbiol Biotechnol 26:89–98. https://doi.org/10.4014/jmb.1505.05008
Liu Y, Sun Q, Li J, Lian B (2018) Bacterial diversity among the fruit bodies of ectomycorrhizal and saprophytic fungi and their corresponding hyphosphere soils. Sci Rep11672.https://doi.org/10.1038/s41598-018-30120-6
Martins SJ, Trexler RV, Vieira FR et al. (2020) Comparing approaches for capturing bacterial assemblages associated with symptomatic (bacterial blotch) and asymptomatic mushroom (Agaricus bisporus) Caps. 4:90–99. https://doi.org/10.1094/pbiomes-08-19-0044-r
Oh S, Lim YW (2018) Effect of fairy ring bacteria on the growth of Tricholoma matsutake in vitro culture. Mycorrhiza 28:411–419. https://doi.org/10.1007/s00572-018-0828-x
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Pent M, Põldmaa K, Bahram M (2017) Bacterial communities in boreal forest mushrooms are shaped both by soil parameters and host identity. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00836
Pent M, Hiltunen M, Põldmaa K et al (2018) Host genetic variation strongly influences the microbiome structure and function in fungal fruiting-bodies. Environ Microbiol 20:1641–1650. https://doi.org/10.1111/1462-2920.14069
Pent M, Bahram M, Põldmaa K (2020) Fruitbody chemistry underlies the structure of endofungal bacterial communities across fungal guilds and phylogenetic groups. ISME J 14:2131–2141. https://doi.org/10.1038/s41396-020-0674-7
Philippe V, Achim Q, Marie D, Amandine LV, Alexis D (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206. https://doi.org/10.1111/nph.13312
Pitt JI, Hocking AD (2009) Fungi and Food Spoilage. Springer, Boston, MA. https://doi.org/10.1007/978-3-030-85640-3
Qu SX, Li HP, Ma L, Hou LJ, Lin JS, Song JD, Hong XYJJoSPR (2015) Effects of different edible mushroom hosts on the development, reproduction and bacterial community of Tyrophagus putrescentiae (Schrank). 61:70–75. https://doi.org/10.1016/j.jspr.2014.12.003
Rivera CS, Blanco D, Oria R, Venturini ME (2010) Diversity of culturable microorganisms and occurrence of Listeria monocytogenes and Salmonella spp. in Tuber aestivum and Tuber melanosporum ascocarps. Food Microbiol 27:286–293. https://doi.org/10.1016/j.fm.2009.11.001
Sanjay AB, Aurélie D, Van Nostrand JD et al (2014) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16:2831–2847. https://doi.org/10.1111/1462-2920.12294
Selim S, Negrel J, Govaerts C, Gianinazzi S, Van Tuinen D (2005) Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the Sorghum mycorrhizosphere. Appl Environ Microbiol 71:6501–6507. https://doi.org/10.1128/AEM.71.11.6501-6507.2005
Simpson GL, Solymos P, Stevens M, Wagner H (2015) Vegan: community ecology package. Time Int 1997:15–17
Singdevsachan SK, Auroshree P, Mishra J, Baliyarsingh B, Tayung K, Thatoi H (2016) Mushroom polysaccharides as potential prebiotics with their antitumor and immunomodulating properties: a review. Bioact Carbohydrates Diet Fibre 7:1–14. https://doi.org/10.1016/j.bcdf.2015.11.001
Splivallo R, Vahdatzadeh M, Maciá-Vicente JG et al (2019) Orchard conditions and fruiting body characteristics drive the microbiome of the black truffle Tuber aestivum. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01437
Tarkka MT, Drigo B, Deveau A (2018) Mycorrhizal microbiomes. Mycorrhiza 28:403–409. https://doi.org/10.1007/s00572-018-0865-5
Timonen S, Jørgensen KS, Haahtela K, Sen R (1998) Bacterial community structure at defined locations of Pinus sylvestris. Can J Microbiol 44:499–513. https://doi.org/10.1139/w98-035
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang Y-H, Hou L-L, Wu X-Q, Zhu M-L, Dai Y, Zhao Y-J (2021) Mycorrhiza helper bacterium Bacillus pumilus HR10 improves growth and nutritional status of Pinus thunbergii by promoting mycorrhizal proliferation. Tree Physiol 42:907–918. https://doi.org/10.1093/treephys/tpab139
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697. https://doi.org/10.1128/jb.173.2.697-703.1991
Wu X-Q, Hou L-L, Sheng J-M, Ren J-H, Zheng L, Chen D, Ye J-R (2012) Effects of ectomycorrhizal fungus Boletus edulis and mycorrhiza helper Bacillus cereus on the growth and nutrient uptake by Pinus thunbergii. Biol Fertil Soils 48:385–391. https://doi.org/10.1007/s00374-011-0638-1
Xiang Q, Luo L, Liang Y, Chen Q, Zhang X, Gu Y (2017) The diversity, growth promoting abilities and anti-microbial activities of bacteria isolated from the fruiting body of Agaricus bisporus. Pol J Microbiol 66:201–207. https://doi.org/10.5604/01.3001.0010.7837
Xing R, Yan H, Gao Q, Zhang F, Wang J, Chen S (2018) Microbial communities inhabiting the fairy ring of Floccularia luteovirens and isolation of potential mycorrhiza helper bacteria. J Basic Microbiol 58:554–563. https://doi.org/10.1002/jobm.201700579
Xing R, Gao Q-b, Zhang F-q, Wang J-l, Shi-long C (2019a) Bacterial community in cold and alkaline environments of Hoh Xil basin in Qinghai-Tibet Plateau and isolation of potential sources of microbiota. Ann Microbiol 69:567–576. https://doi.org/10.1007/s13213-019-01447-w
Xing R, Gao Qb, Zhang Fi, Wang J, Chen S (2019b) Large-scale distribution of bacterial communities in the Qaidam Basin of the Qinghai–Tibet Plateau. Microbiol Open https://doi.org/10.1002/mbo3.909
Zambonelli A, Gregory M (2012) Edible ectomycorrhizal mushrooms. Soil Biology 34:105–124. https://doi.org/10.1007/978-3-642-33823-6
Zarenejad F, Yakhchali B, Rasooli I (2012) Evaluation of indigenous potent mushroom growth promoting bacteria (MGPB) on Agaricus bisporus production. World J Microbiol Biotechnol 28:99–104. https://doi.org/10.1007/s11274-011-0796-1
Zhou J, Bai X, Zhao R (2017) Microbial communities in the native habitats of Agaricus sinodeliciosus from Xinjiang Province revealed by amplicon sequencing. Sci Rep. https://doi.org/10.1038/s41598-017-16082-1
Funding
This study received financial support from the Sanjiangyuan National Park Joint Program (LHZX-2020–02-01); Special Fund for Qilian Mountain National Park (QHTX-2020–004); Long-Term National Scientific Research Base of Qilian Mountain National Park, Xining 810000, Qinghai, China; the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA2005010406); and Construction Project for Innovation Platform of Qinghai province (2022-ZJ-Y04).
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Rui Xing was the primary investigator of the original study. Hai-Chen Zhang was involved in fieldwork and laboratory analyses and manuscript writing. Xiao-Feng Chi was involved in fieldwork. Fa-qi Zhang and Qing-bo Gao were involved in laboratory analyses. Shi-long Chen is involved in supervision. All authors take responsibility for the reliability and accuracy of data, data analyses, and approval of the final version of the manuscript.
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Xing, R., Zhang, HC., Gao, Qb. et al. Bacterial communities associated with mushrooms in the Qinghai-Tibet Plateau are shaped by soil parameters. Int Microbiol 26, 231–242 (2023). https://doi.org/10.1007/s10123-022-00286-1
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DOI: https://doi.org/10.1007/s10123-022-00286-1