Cistus ladanifer scrublands, traditionally considered as unproductive, have nonetheless been observed to produce large quantities of king bolete (Boletus edulis) fruitbodies. These pyrophytic scrublands are prone to wildfires, which severely affect fungi, hence the need for fire prevention in producing C. ladanifer scrublands. In addition, B. edulis productions have severely decreased in the last years. A deeper understanding of the B. edulis life cycle and of biotic and abiotic factors influencing sporocarp formation is needed to implement management practices that facilitate B. edulis production. For example, some bacteria likely are involved in sporocarp production, representing a key part in the triple symbiosis (plant-fungus-bacteria). In this study, we used soil DNA metabarcoding in C. ladanifer scrublands to (i) assess the effect of site history and fire prevention treatment on bacterial richness and community composition; (ii) test if there was any correlation between various taxonomic groups of bacteria and mycelial biomass and sporocarp production of B. edulis; and to (iii) identify indicator bacteria associated with the most productive B. edulis sites. Our results show that site history drives bacterial richness and community composition, while fire prevention treatments have a weaker, but still detectable effect, particularly in the senescent plots. Sporocarp production correlated positively with genera in Verrucomicrobia. Several genera, e.g. Azospirillum and Gemmatimonas, were identified as indicators of the most productive sites, suggesting a potential biological role in B. edulis fructification. This study provides a better understanding of the triple symbiosis (plant-fungus-bacteria) involved in C. ladanifer-B. edulis systems.

Biodiversity Dynamics Research Group Naturalis Biodiversity Center Vondellaan 55 PO Box 9517 2300 RA Leiden The Netherlands

Fire and Applied Mycology Laboratory Departments of Agroforestry Sciences and Vegetal Production and Natural Resources Sustainable Forest Management Research Institute University of Valladolid Avda Madrid 44 34071 Palencia Spain

IDForest Biotecnología Forestal Aplicada Calle Curtidores 17 34004 Palencia Spain

Laboratory of Environmental Microbiology Institute of Microbiology of the CAS Vídeňská 1083 14220 Praha 4 Czech Republic

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Allison, S.D. , Hanson, C.A. , and Treseder, K.K. (2007) Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol Biochem 39: 1878–1887.

Anderson, M.J. (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26: 32–46.

Antony‐Babu, S. , Deveau, A. , Nostrand, J.D. , Van Zhou, J. , Tacon, F. , Le Robin, C. , et al (2013) Black truffle‐associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16: 2831–2847. PubMed

Baath, E. , Frostegard, A.S.A. , Pennanen, T. , and Fritze, H. (1995) Microbial community structure and pH response in relation to soil organic matter quality in wood‐ash fertilized, clear‐cut or burned coniferous forest soils. Soil Biol Biochem 21: 229–240.

Baldrian, P. (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41: 109–130. PubMed

Baldrian, P. , Kolarik, M. , Stursova, M. , Kopecky, J. , Valaskova, V. , Vetrovsky, T. , et al (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6: 248–258. PubMed PMC

Barbieri, E. , Bertini, L. , Rossi, I. , Ceccaroli, P. , Saltarelli, R. , Guidi, C. , et al (2005) New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiol Lett 247: 23–35. PubMed

Blaha, D. , Prigent‐Combaret, C. , Mirza, M.S. , and Moënne‐Loccoz, Y. (2006) Phylogeny of the 1‐aminocyclopropane‐1‐carboxylic acid deaminase‐ encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56: 455–470. PubMed

Boer, W. , De Folman, L.B. , Summerbell, R.C. , and Boddy, L. (2005) Living in a fungal world: impact of fungi on soil bacterial. FEMS Microbiol Rev 29: 795–811. PubMed

Bonfante, P. , and Anca, I. (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63: 363–383. PubMed

Buckley, D.H. , and Schmidt, T.M. (2001) Environmental factors influencing the distribution of rRNA from Verrucomicrobia in soil. FEMS Microbiol Ecol 35: 105–112. PubMed

Buée, M. , Reich, M. , Murat, C. , Morin, E. , Nilsson, R.H. , Uroz, S. , and Martin, F. (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184: 449–456. PubMed

Caporaso, J.G. , Lauber, C.L. , Walters, W.A. , Berg‐Lyons, D. , Lozupone, C.A. , Tumbaugh, P.J. , et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108: 4516–4522. PubMed PMC

Caporaso, J.G. , Lauber, C.L. , Walters, W.A. , Berg‐Lyons, D. , Huntley, J. , Fierer, N. , et al (2012) Ultra‐high‐throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621–1624. PubMed PMC

Carter, M.C. , and Foster, C.D. (2004) Prescribed burning and productivity in southern pine forests: a review. For Ecol Manage 191: 93–109.

Catcheside, P.S. , and Catcheside, D.E.A. (2012) Boletus edulis (Boletaceae), a new record for Australia. J Adelaide Bot Gard 25: 5–10.

Certini, G. (2005) Effects of fire on properties of forest soils: a review. Oecologia 143: 1–10. PubMed

Choromanska, U. , and DeLuca, T.H. (2001) Prescribed fire alters the impact of wildfire on soil biochemical properties in a Ponderosa pine forest. Soil Sci Soc Am J 65: 232–238.

Cole, J.R. , Wang, Q. , Cardenas, E. , Fish, J. , Chai, B. , Farris, R.J. , et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: 141–145. PubMed PMC

Comandini, O. , Contu, M. , and Rinaldi, A.C. (2006) An overview of Cistus ectomycorrhizal fungi. Mycorrhiza 16: 381–395. PubMed

Creus, C.M. , Graziano, M. , Casanovas, E.M. , Pereyra, M.A. , Simontacchi, M. , Puntarulo, S. , et al (2005) Nitric oxide is involved in the Azospirillum brasilense‐induced lateral root formation in tomato. Planta 221: 297–303. PubMed

de Boer, W. (2017) Upscaling of fungal–bacterial interactions: from the lab to the field. Curr Opin Microbiol 37: 35–41. PubMed

Dedysh, S.N. and Kulichevskaya, I.S. (2014) Acidophilic planctomycetes: Expanding the horizons of new planctomycete diversity In Planctomycetes: Cell Structure. Fuerst J.A. (ed.). New York, NY, USA: Humana Press, Origins and Biology, pp. 125–139.

Dentinger, B.T.M. , Ammirati, J.F. , Both, E.E. , Desjardin, D.E. , Halling, R.E. , Henkel, T.W. , et al (2010) Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). Mol Phylogenet Evol 57: 1276–1292. PubMed

Deveau, A. , Antony‐Babu, S. , Le Tacon, F. , Robin, C. , Frey‐Klett, P. , and Uroz, S. (2016) Temporal changes of bacterial communities in the Tuber melanosporum ectomycorrhizosphere during ascocarp development. Mycorrhiza 26: 389–399. PubMed

Dufrêne, M. , and Legendre, P. (1997) Species assemblages and indicator species: the need for a flexible assymetrical approach. Ecol Monogr 67: 345–366.

Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461. PubMed

Felske, A. , Wolterink, A. , van Lis, R. , de Vos, W.M. , and Akkermans, A.D.L. (1999) Searching for predominant soil bacteria: 16S rDNA cloning versus strain cultivation. FEMS Microbiol Ecol 30: 137–145. PubMed

Fierer, N. , Ladau, J. , Clemente, J.C. , Leff, J.W. , Owens, S.M. , Pollard, K.S. , et al (2013) Reconstructing the microbial diversity and function of pre‐agricultural tallgrass prairie soils in the United States. Science 342: 621–624. PubMed

Frey, S.D. , Knorr, M. , Parrent, J.L. , and Simpson, R.T. (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage 196: 159–171.

Frey‐Klett, P. , Garbaye, J. , and Tarkka, M. (2007) The mycorrhiza helper bacteria revisited. New Phytol 176: 22–36. PubMed

Hardoim, P.R. , van Overbeek, L.S. , Berg, G. , Pirttilä, M. , Compant, S. , Campisano, A. , and Döring, M. (2015) The Hidden World within Plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79: 293–320. PubMed PMC

Hernández‐Rodríguez, M. , Oria‐de‐Rueda, J.A. , and Martín‐Pinto, P. (2013) Post‐fire fungal succession in a Mediterranean ecosystem dominated by Cistus ladanifer L. For Ecol Manage 289: 48–57.

Hernández‐Rodríguez, M. , de Miguel, S. , Pukkala, T. , Oria‐de‐Rueda, J.A. , and Martín‐Pinto, P. (2015a) Climate‐sensitive models for mushroom yields and diversity in Cistus ladanifer scrublands. Agric For Meteorol 213: 173–182.

Hernández‐Rodríguez, M. , Oria‐de‐Rueda, J.A. , Pando, V. , and Martín‐Pinto, P. (2015b) Impact of fuel reduction treatments on fungal sporocarp production and diversity associated with Cistus ladanifer L. ecosystems. For Ecol Manage 353: 10–20.

Hernández‐Rodríguez, M. , Martín‐Pinto, P. , Oria‐de‐Rueda, J.A. , and Diaz‐Balteiro, L. (2017) Optimal management of Cistus ladanifer shrublands for biomass and Boletus edulis mushroom production. Agroforest Syst 91: 663–676.

Honrubia, M. (2009) Las micorrizas: una relación planta‐hongo que dura más de 400 millones de años. An del Jardín Botánico Madrid 66: 133–144.

Jiménez‐Esquilín, A.E. , Stromberger, M.E. , Massman, W.J. , Frank, J.M. , and Shepperd, W.D. (2007) Microbial community structure and activity in a Colorado Rocky Mountain forest soil scarred by slash pile burning. Soil Biol Biochem 39: 1111–1120.

Kaiser, O. , Pühler, A. , and Selbitschka, W. (2001) Phylogenetic analysis of microbial diversity in the rhizoplane of oilseed rape (Brassica napus cv. Westar) employing cultivation‐dependent and cultivation‐independent approaches. Microb Ecol 42: 136–149. PubMed

Krieg, N.R. , Staley, J.T. , Brown, D.R. , Hedlund, B.P. , Paster, B.J. , Ward, N.L. , et al (2010) Bergey′s Manual of Systematic Bacteriology, 2nd edn New York, Dordrecht, Heidelberg, London: Springer.

Lauber, C.L. , Strickland, M.S. , Bradford, M.A. , and Fierer, N. (2008) The influence of soil properties on the structure of bacterial and fungal communities across land‐use types. Soil Biol Biochem 40: 2407–2415.

Lauber, C.L. , Hamady, M. , Knight, R. , and Fierer, N. (2009) Pyrosequencing‐based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75: 5111–5120. PubMed PMC

Lladó, S. , López‐Mondéjar, R. , and Baldrian, P. (2017) Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol Rev 81: 1–27. PubMed PMC

Martín‐Pinto, P. , Vaquerizo, H. , Peñalver, F. , Olaizola, J. , and Oria‐de‐Rueda, J.A. (2006) Early effects of a wildfire on the diversity and production of fungal communities in Mediterranean vegetation types dominated by Cistus ladanifer and Pinus pinaster in Spain. For Ecol Manage 225: 296–305.

Mediavilla, O. , Olaizola, J. , Santos‐Del‐Blanco, L. , Oria‐De‐Rueda, J.A. , and Martín‐Pinto, P. (2016) Mycorrhization between Cistus ladanifer L. and Boletus edulis Bull is enhanced by the mycorrhiza helper bacteria Pseudomonas fluorescens Migula. Mycorrhiza 26: 161–168. PubMed

Mediavilla, O. , Hernández‐Rodríguez, M. , Olaizola, J. , Santos‐del‐Blanco, L. , Oria‐de‐Rueda, J.A. , and Martín‐Pinto, P. (2017) Insights into the dynamics of Boletus edulis mycelium and fruiting after fire prevention management. For Ecol Manage 404: 108–114.

Nacke, H. , Thürmer, A. , Wollherr, A. , Will, C. , Hodac, L. , Herold, N. , et al (2011) Pyrosequencing‐based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS ONE 6: e17000. PubMed PMC

Oria‐de‐Rueda, J.A. , Martín‐Pinto, P. , and Olaizola, J. (2008) Bolete productivity of Cistaceous scrublands in Northwestern Spain. Econ Bot 62: 323–330.

Pent, M. , Põldmaa, K. , and Bahram, M. (2017) Bacterial communities in Boreal forest mushrooms are shaped both by soil parameters and host identity. Front Microbiol 8: 836. PubMed PMC

R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

Reich, P.B. , Peterson, D.W. , Wedin, D.A. , and Wrage, K. (2001) Fire and vegetation effects on productivity and N cycling across a forest–grassland continuum. Ecology 82: 1703–1719.

Rousk, J. , Baath, E. , Brookes, P.C. , Lauber, C.L. , Lozupone, C. , Caporaso, J.G. , et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4: 1340–1351. PubMed

Santillán, E. , Seshan, H. , Constancias, F. , Drautz‐Moses, D.I. and Wuertz, S. (2018) Frequency of disturbance alters diversity, function, and underlying assembly mechanisms of complex bacterial communities. bioRxiv 5: 8 10.1101/313585 PubMed DOI PMC

Savoie, J.M. , and Largeteau, M.L. (2011) Production of edible mushrooms in forests: trends in development of a mycosilviculture. Appl Microbiol Biotechnol 89: 971–979. PubMed

Shen, C. , Xiong, J. , Zhang, H. , Feng, Y. , Lin, X. , Li, X. , et al (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57: 204–211.

Shen, J. , Chen, C.R. and Lewis, T. (2016) Long term repeated fire disturbance alters soil bacterial diversity but not the abundance in an Australian wet sclerophyll forest. Sci Rep 6: 19639. PubMed PMC

Smith, N.R. , Kishchuk, B.E. , and Mohn, W.W. (2008) Effects of wildfire and harvest disturbances on forest soil bacterial communities. Appl Environ Microbiol 74: 216–224. PubMed PMC

Soil Survey Staff (2010) Keys to Soil Taxonomy, 11th edn Washington, DC: Soil Survey Staff.

Splivallo, R. , Deveau, A. , Valdez, N. , Kirchhoff, N. , Frey‐Klett, P. , and Karlovsky, P. (2015) Bacteria associated with truffle‐fruiting bodies contribute to truffle aroma. Environ Microbiol 17: 2647–2660. PubMed

Steenhoudt, O. , and Vanderleyden, J. (2000) Azospirillum, a free‐living nitrogen‐fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24: 487–506. PubMed

Sun, S. , Li, S. , Avera, B.N. , Strahm, B.D. and Badgley, B.D. (2017) Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. Appl Environ Microbiol 83: pii: e00966‐17. PubMed PMC

Taylor, A.F.S. (2002) Fungal diversity in ectomycorrhizal communities: sampling effort and species detection. Plant Soil 244: 19–28.

Yang, Y. , Wang, N. , Guo, X. , Zhang, Y. , and Ye, B. (2017) Comparative analysis of bacterial community structure in the rhizosphere of maize by highthroughput pyrosequencing. PLoS ONE 12: e0178425. PubMed PMC

Zhang, X. , Liu, S. , Li, X. , Wang, J. , Ding, Q. , Wang, H. , et al (2016) Changes of soil prokaryotic communities after clear‐cutting in a karst forest: evidences for cutting‐based disturbance promoting deterministic processes. FEMS Microbiol Ecol 92: pii: fiw026. PubMed

Zinger, L. , Lejon, D.P.H. , Baptist, F. , Bouasria, A. , Aubert, S. , Geremia, R.A. , and Choler, P. (2011) Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS ONE 6: e0019950. PubMed PMC

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DQ768106, AJ229235, FN400860, EF457384, AJ535711, AB072735, CP001854, AY324110, HM214537, X97098, AJ401115, FJ177532, EF457390, EF457407, MK323080, MK325185