Abstract
Here, we investigated the influence of Chinese white truffle (Tuber panzhihuanense) symbioses on the microbial communities associated with Corylus avellana during the early development stage of symbiosis. The microbial communities associated with ectomycorrhizae, and associated with roots without T. panzhihuanense colonization, were determined via high-throughput sequencing of bacterial 16S rRNA genes and fungal ITS genes. Microbial community diversity was higher in the communities associated with the ectomycorrhizae than in the control treatment. Further, bacterial and fungal community structures were different in samples containing T. panzhihuanense in association with C. avellana compared to the control samples. In particular, the bacterial genera Rhizobium, Pedomicrobium, and Herbiconiux were more abundant in the ectomycorrhizae, in addition to the fungal genus Monographella. Moreover, there were clear differences in some physicochemical properties among the rhizosphere soils of the two treatments. Statistical analyses indicated that soil properties including exchangeable magnesium and exchangeable calcium prominently influenced microbial community structure. Lastly, inference of bacterial metabolic functions indicated that sugar and protein metabolism functions were significantly more enriched in the communities associated with the ectomycorrhizae from C. avellana mycorrhized with T. panzhihuanense compared to communities from roots of cultivated C. avellana without T. panzhihuanense. Taken together, these results highlight the interactions among ectomycorrhizal fungi, soil properties, and microbial communities that are associated with host plants and further our understanding of the ecology and cultivation of the economically important T. panzhihuanense truffles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alonso PR, Ágreda T, Águeda B, Aldea J, Martínez-Peña F, Modrego MP (2014) Soil physical properties influence "black truffle" fructification in plantations. Mycorrhiza 24(S1):S55–S64. https://doi.org/10.1007/s00572-014-0558-7
Barbieri E, Guidi C, Bertaux J, Freyklett P, Garbaye J, Ceccaroli P, Saltarelli R, Zambonelli A, Stocchi V (2007) Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environ Microbiol 9(9):2234–2246. https://doi.org/10.1111/j.1462-2920.2007.01338.x
Belfiori B, Riccioni C, Paolocci F, Rubini A (2016) Characterization of the reproductive mode and life cycle of the whitish truffle T. borchii. Mycorrhiza 26(6):515–527. https://doi.org/10.1007/s00572-016-0689-0
Benucci GM, Gógán CA, Falini LB, Bencivenga M, Massimo GD, Donnini D (2012) Mycorrhization of Quercus robur L., Quercus cerris L. and Corylus avellana L. seedlings with Tuber macrosporum Vittad. Mycorrhiza 22(8):639–646. https://doi.org/10.1007/s00572-012-0441-3
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol 79(8):2519–2526. https://doi.org/10.1128/AEM.03870-12
Bonito GM, Gryganskyi AP, Trappe JM, Vilgalys R (2010) A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal. Mol Ecol 19(22):4994–5008. https://doi.org/10.1111/j.1365-294X.2010.04855.x
Bonito G, Brenneman T, Vilgalys R (2011) Ectomycorrhizal fungal diversity in orchards of cultivated pecan (Carya illinoinensis; Juglandaceae). Mycorrhiza 21(7):601–612. https://doi.org/10.1007/s00572-011-0368-0
Bradshaw BP (2005) Physiological aspects of Corylus avellana associated with the French black truffle fungus Tuber melanosporum and the consequence for commercial production of black truffles in Western Australia. Dissertation, School of Biological Sciences and Biotechnology Murdoch University
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen YL (2002) Cultivation techniques for European truffles (Tuber spp.). Edible Fungi of China
Deveau A, Antony-Babu S, Le TF, Robin C, Frey-Klett P, Uroz S (2016) Temporal changes of bacterial communities in the Tuber melanosporum ectomycorrhizosphere during ascocarp development. Mycorrhiza 26(5):389–399. https://doi.org/10.1007/s00572-015-0679-7
Dominguez JA, Martin A, Anriquez A, Albanesi A (2012) The combined effects of Pseudomonas fluorescens and Tuber melanosporum on the quality of Pinus halepensis seedlings. Mycorrhiza 22(6):429–436. https://doi.org/10.1007/s00572-011-0420-0
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(2460–1):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Esmaeili TA, Chatterton S, Gossen B, Mclaren D (2017) Metagenomic analysis of oomycete communities from the rhizosphere of field pea on the Canadian prairies. Can J Microbiol 63:758–768. https://doi.org/10.1139/cjm-2017-0099
Garcíamontero LG, Casermeiro MA, Hernando J, Hernando I (2006) Soil factors that influence the fruiting of Tuber melanosporum (black truffle). Aust J Soil Res 44(8):731–738. https://doi.org/10.1071/SR06046
Garcíamontero LG, Quintana A, Valverdeasenjo I, Díaz P (2009) Calcareous amendments in truffle culture: a soil nutrition hypothesis. Soil Biol Biochem 41(6):1227–1232. https://doi.org/10.1016/j.soilbio.2009.03.003
Healy RA, Zurier H, Bonito G, Smith ME, Pfister DH (2016) Mycorrhizal detection of native and non-native truffles in a historic arboretum and the discovery of a new North American species, Tuber arnoldianum sp. nov. Mycorrhiza 26(7):781–792. https://doi.org/10.1007/s00572-016-0713-4
Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187(4):895–910. https://doi.org/10.1111/j.1469-8137.2010.03399.x
Kirk P, Cannon P, Minter D, Stalpers J (2008) Dictionary of the Fungi. Commonwealth Mycol Inst 106:507–508
Kües U, Martin F (2011) On the road to understanding truffles in the underground. Fungal Genet Biol 48(6):555–560. https://doi.org/10.1016/j.fgb.2011.02.002
Langenheder S, Székely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. IMSE J 5(7):1086–1094. https://doi.org/10.1038/ismej.2010.207
Langille MGI, Zaneveld J, Caporaso JG, Mcdonald D, Dan K, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lefevre C (2012) Native and cultivated truffles of North America. Springer Berl Heid 34:209–226. https://doi.org/10.1007/978-3-642-33823-6_12
Lefevre C, Hall I (2001) The status of truffle cultivation: a global perspective. Acta Hortic 556(556):513–520. https://doi.org/10.17660/ActaHortic.2001.556.75
Lenoir I, Fontaine J, Lounès-Hadj SA (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15. https://doi.org/10.1016/j.phytochem.2016.01.002
Li Q, Li X, Chen C, Li S, Huang W, Xiong C, Jin X, 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(1):89–98. https://doi.org/10.4014/jmb.1505.05008
Li Q, Zhao J, Xiong C, Li X, Chen Z, Li P, Huang W (2017) Tuber indicum shapes the microbial communities of ectomycorhizosphere soil and ectomycorrhizae of an indigenous tree (Pinus armandii). PLoS One 12(4):e0175720. https://doi.org/10.1371/journal.pone.0175720
Ling L, U X (2013) Endophytes research progress and application prospect. Journal of Anhui agricultural sciences
Liu P, Liu G, Cheng Y, Wang Y, Deng JX (2013) A new white truffle species, Tuber panzhihuanense from China. Mycol Prog 12(3):557–561. https://doi.org/10.1007/s11557-012-0862-6
Liu CY, Yang M, Tang P, Li XL, Xiao YJ, Xiao LY, Zheng, and Wang Y (2014) Research on mycorrhizal seedling cultivation and microstructure of Tuber panzhihuanense. Edible Fungi of China
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Ludwigmüller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37(7):1325–1334. https://doi.org/10.1007/s10529-015-1814-4
Marozzi G, Sánchez S, Benucci GMN, Bonito G, Falini LB, Albertini E, Donnini D (2017) Mycorrhization of pecan (Carya illinoinensis) with black truffles: Tuber melanosporum and Tuber brumale. Mycorrhiza 27(3):303–309. https://doi.org/10.1007/s00572-016-0743-y
Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464(7291):1033–1038. https://doi.org/10.1038/nature08867
Mello A, Miozzi L, Vizzini A, Napoli C, Kowalchuk G, Bonfante P (2010) Bacterial and fungal communities associated with Tuber magnatumâ-productive niches. G Bot Ital 144:323–332. https://doi.org/10.1080/11263500903374724
Mello A, Ding GC, Piceno YM, Napoli C, Tom LM, Desantis TZ, Andersen GL, Smalla K, Bonfante P (2013) Truffle brûlés have an impact on the diversity of soil bacterial communities. PLoS One 8(4):e61945. https://doi.org/10.1371/journal.pone.0061945
Page AL, Miller RH, Dennis RK (1982) Methods of soil analysis. Catena 15:99–100. https://doi.org/10.1007/BF02869702
Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18(5):1403–1414. https://doi.org/10.1111/1462-2920.13023
Ruma K, Sunil K, Prakash HS (2014) Bioactive potential of endophytic Myrothecium sp. isolate M1-CA-102, associated with Calophyllum apetalum. Pharm Biol 52(6):665–676. https://doi.org/10.3109/13880209.2013.863950
Salerni E, Iotti M, Leonardi P, Gardin L, Aguanno MD, Perini C, Pacioni P, Zambonelli A (2014) Effects of soil tillage on Tuber magnatum development in natural truffières. Mycorrhiza 24(S1):S79–S87. https://doi.org/10.1007/s00572-013-0543-6
Shu-Chao LI, Qiao P, Liu S S, Chen J, Guo S X (2017) Research progress in the molecular systematics and symbiotic mechanism of Tuber (Tuberaceae, Ascomycota. Mycosystema
Splivallo R, Deveau A, Valdez N, Kirchhoff N, Frey Klett P, Karlovsky P (2015) Bacteria associated with truffle-fruiting bodies contribute to truffle aroma. Environ Microbiol 17(8):2647–2660. https://doi.org/10.1111/1462-2920.12521
Streiblová E, Gryndlerová H, Gryndler M (2012) Truffle brûlé: an efficient fungal life strategy. FEMS Microbiol Ecol 80(1):1–8. https://doi.org/10.1111/j.1574-6941.2011.01283.x
Tang, P (2005) A study of truffle resources and optimal Nichesin Panzhihua region. J Sichuan For Sci Technol
Team, R D C, (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, v 1, p. 12–21
Ulery AL, Drees LR (2008) Methods of soil analysis. Catena 15(1):99–100
Vahdatzadeh M, Deveau A, Splivallo R (2015) The role of the microbiome of truffles in aroma formation: a meta-analysis approach. Appl Environ Microbiol 81(20):6946–6952. https://doi.org/10.1128/AEM.01098-15
Wan SP, Liu PG (2014) Diversity of culturable bacteria associated with Ascocarps of a Chinese white truffle, Tuber panzhihuanense (Ascomycota). Plant Divers Res 36:29–36
Wan SP, Yu FQ, Tang L, Wang R, Wang Y, Liu PG, Wang XH, Zheng Y (2015a) Ectomycorrhizae of Tuber huidongense and T. liyuanum with Castanea mollissima and Pinus armandii. Mycorrhiza 26(3):249–256. https://doi.org/10.1007/s00572-015-0663-2
Wan SP, Zheng Y, Tang L, Wang R, Liu PG, Yu FQ (2015b) Diversity of culturable bacteria associated with Tuber panzhihuanense-Pinus armandii Ectomycorrhizosphere soil. Plant Divers Res 37(06):861–870
Wang YA, Zhao XS, Yin BZ, Zhen WC, Guo JT (2015) Biochemical defenses induced by mycorrhizae fungi Glomus Mosseae in controlling strawberry Fusarium wilt. Open Biomed Eng J 9(1):301–304. https://doi.org/10.2174/1874120701509010301
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227. https://doi.org/10.1038/nature11053
Zhang L, Kang M, Huang Y, Yang L (2016) Fungal communities from the calcareous deep-sea sediments in the Southwest India ridge revealed by Illumina sequencing technology. World J Microbiol Biotechnol 32(5):78. https://doi.org/10.1007/s11274-016-2030-7
Zhou J, Wei H (2013) rDNA-ITS sequence analysis identify truffle-associated Fungi. J Xinyang Normal Univ
Acknowledgments
We would like to thank LetPub (www.letpub.com) for providing linguistic assistance during the preparation of this manuscript.
Funding
This work was supported by the Science and Technology Support Project in Sichuan Province (2016NYZ0040) and the Sichuan Mushroom Innovation Team.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This research does not involve human participants and/or animals.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yang, M., Zou, J., Liu, C. et al. Chinese white truffles shape the ectomycorrhizal microbial communities of Corylus avellana. Ann Microbiol 69, 553–565 (2019). https://doi.org/10.1007/s13213-019-1445-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-019-1445-4