Regional biogeography versus intra-annual dynamics of the root and soil microbiome
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
DE-SC0014108
U.S. Department of Energy
DE-SC0018409
U.S. Department of Energy
DE-SC0018409
U.S. Department of Energy
DE-SC0018409
U.S. Department of Energy
DE-SC0014108
U.S. Department of Energy
DE-SC0014108
U.S. Department of Energy
DE-SC0014108
U.S. Department of Energy
DEB 1832042
U.S. National Science Foundation
DEB 1832042
U.S. National Science Foundation
PubMed
37287059
PubMed Central
PMC10245661
DOI
10.1186/s40793-023-00504-x
PII: 10.1186/s40793-023-00504-x
Knihovny.cz E-zdroje
- Klíčová slova
- Panicum virgatum, Plant microbiome, Root bacteria, Root fungi, Soil bacteria, Soil fungi,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). RESULTS: To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. CONCLUSIONS: Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.
Department of Integrative Biology Michigan State University East Lansing MI USA
Department of Microbiology and Molecular Genetics Michigan State University East Lansing MI USA
Department of Plant Soil and Microbial Sciences Michigan State University East Lansing MI USA
The Great Lakes Bioenergy Research Center Michigan State University East Lansing MI USA
W K Kellogg Biological Station Michigan State University Hickory Corners MI USA
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Kuzyakov Y, Blagodatskaya E. Microbial hotspots and hot moments in soil: Concept & review. Soil Biol Biochem. 2015;83:184–99. doi: 10.1016/j.soilbio.2015.01.025. DOI
Crowther TW, van den Hoogen J, Wan J, Mayes MA, Keiser AD, Mo L, et al. The global soil community and its influence on biogeochemistry. Science. 2019;365(6455):eaav0550. doi: 10.1126/science.aav0550. PubMed DOI
Fierer N, Jackson RB. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA. 2006;103(3):626–31. doi: 10.1073/pnas.0507535103. PubMed DOI PMC
Větrovský T, Kohout P, Kopecký M, Machac A, Man M, Bahnmann BD, et al. A meta-analysis of global fungal distribution reveals climate-driven patterns. Nat Commun. 2019;10(1):5142. doi: 10.1038/s41467-019-13164-8. PubMed DOI PMC
Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, et al. Structure and function of the global topsoil microbiome. Nature. 2018;560(7717):233–7. doi: 10.1038/s41586-018-0386-6. PubMed DOI
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, et al. Global diversity and geography of soil fungi. Science. 2014;346(6213). 10.1126/science.1256688. PubMed
Lichter J. Rates of weathering and chemical depletion in soils across a chronosequence of Lake Michigan sand dunes. Geoderma. 1998;85(4):255–82. doi: 10.1016/S0016-7061(98)00026-3. DOI
Keller KR, Lau JA. When mutualisms matter: rhizobia effects on plant communities depend on host plant population and soil nitrogen availability. J Ecol. 2018 doi: 10.1111/1365-2745.12938. DOI
Hannula SE, Kielak AM, Steinauer K, Huberty M, Jongen R, De Long JR, et al. Time after time: temporal variation in the Effects of Grass and Forb Species on Soil Bacterial and Fungal Communities. mBio. 2019;10(6):e02635–19. doi: 10.1128/mBio.02635-19. PubMed DOI PMC
Martinovic T, Odriozola I, Masinova T, Doreen Bahnmann B, Kohout P, Sedlak P, et al. Temporal turnover of the soil microbiome composition is guild-specific. Ecol Lett. 2021;24(12):2726–38. doi: 10.1111/ele.13896. PubMed DOI
Schmidt SK, Nemergut DR, Darcy JL, Lynch R. Do bacterial and fungal communities assemble differently during primary succession? Mol Ecol. 2014;23(2):254–8. doi: 10.1111/mec.12589. PubMed DOI
Zhao M, Sun B, Wu L, Wang F, Wen C, Wang M, et al. Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes. Mol Ecol. 2019;28(7):1842–56. doi: 10.1111/mec.15053. PubMed DOI
Brown SP, Jumpponen A. Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Mol Ecol. 2014;23(2):481–97. doi: 10.1111/mec.12487. PubMed DOI
Li S-p, Wang P, Chen Y, Wilson MC, Yang X, Ma C, et al. Island biogeography of soil bacteria and fungi: similar patterns, but different mechanisms. ISME J. 2020;14(7):1886–96. doi: 10.1038/s41396-020-0657-8. PubMed DOI PMC
Guo X, Feng J, Shi Z, Zhou X, Yuan M, Tao X, et al. Climate warming leads to divergent succession of grassland microbial communities. Nat Clim Change. 2018;8(9):813–8. doi: 10.1038/s41558-018-0254-2. DOI
Nuñez MA, Horton TR, Simberloff D. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology. 2009;90(9):2352–9. doi: 10.1890/08-2139.1. PubMed DOI
Lin Q, Baldrian P, Li L, Novotny V, Heděnec P, Kukla J, et al. Dynamics of Soil Bacterial and Fungal Communities during the secondary succession following Swidden Agriculture IN Lowland forests. Front Microbiol. 2021;12. 10.3389/fmicb.2021.676251. PubMed PMC
Sanford GR, Jackson RD, Booth EG, Hedtcke JL, Picasso V. Perenniality and diversity drive output stability and resilience in a 26-year cropping systems experiment. Field Crops Research. 2021;263:108071. doi: 10.1016/j.fcr.2021.108071. DOI
Zhalnina K, Hawkes C, Shade A, Firestone MK, Pett-Ridge J. Managing Plant Microbiomes for sustainable Biofuel production. Phytobiomes J. 2021;5(1):3–13. doi: 10.1094/pbiomes-12-20-0090-e. DOI
Ruan L, Bhardwaj AK, Hamilton SK, Robertson GP. Nitrogen fertilization challenges the climate benefit of cellulosic biofuels. Environ Res Lett. 2016;11(6):064007. doi: 10.1088/1748-9326/11/6/064007. DOI
Geisseler D, Scow KM. Long-term effects of mineral fertilizers on soil microorganisms – A review. Soil Biol Biochem. 2014;75:54–63. doi: 10.1016/j.soilbio.2014.03.023. DOI
Dai Z, Su W, Chen H, Barberán A, Zhao H, Yu M, et al. Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro‐ecosystems across the globe. Glob Change Biol. 2018;24(8):3452–61. doi: 10.1111/gcb.14163. PubMed DOI
Zhang Ta, Chen HYH, Ruan H. Global negative effects of nitrogen deposition on soil microbes. ISME J. 2018;12(7):1817–25. doi: 10.1038/s41396-018-0096-y. PubMed DOI PMC
Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 2012;6(5):1007–17. doi: 10.1038/ismej.2011.159. PubMed DOI PMC
Li X, Petipas RH, Antoch AA, Liu Y, Stel HV, Bell-Dereske L, et al. Switchgrass cropping systems affect soil carbon and nitrogen and microbial diversity and activity on marginal lands. GCB Bioenergy. 2022;14(8):918–40. doi: 10.1111/gcbb.12949. DOI
Li B-B, Roley SS, Duncan DS, Guo J, Quensen JF, Yu H-Q, et al. Long-term excess nitrogen fertilizer increases sensitivity of soil microbial community to seasonal change revealed by ecological network and metagenome analyses. Soil Biol Biochem. 2021;160:108349. doi: 10.1016/j.soilbio.2021.108349. DOI
Liang Y, Ning D, Lu Z, Zhang N, Hale L, Wu L, et al. Century long fertilization reduces stochasticity controlling grassland microbial community succession. Soil Biol Biochem. 2020;151:108023. doi: 10.1016/j.soilbio.2020.108023. DOI
Tiemann LK, Billings SA. Indirect Effects of Nitrogen amendments on Organic substrate quality increase enzymatic activity driving decomposition in a Mesic Grassland. Ecosystems. 2011;14(2):234–47. doi: 10.1007/s10021-010-9406-6. DOI
Robertson GP, Hamilton SK, Barham BL, Dale BE, Izaurralde RC, Jackson RD, et al. Cellulosic biofuel contributions to a sustainable energy future: choices and outcomes. Science. 2017;356(6345). 10.1126/science.aal2324. PubMed
Hestrin R, Lee MR, Whitaker BK, Pett-Ridge J. The switchgrass microbiome: a review of structure, function, and taxonomic distribution. Phytobiomes J. 2021;5(1):14–28. doi: 10.1094/pbiomes-04-20-0029-fi. DOI
Gelfand I, Sahajpal R, Zhang X, Izaurralde RC, Gross KL, Robertson GP. Sustainable bioenergy production from marginal lands in the US Midwest. Nature. 2013;493:514. doi: 10.1038/nature11811. PubMed DOI
Roley SS, Duncan DS, Liang D, Garoutte A, Jackson RD, Tiedje JM, et al. Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient. PLoS ONE. 2018;13(6):e0197320. doi: 10.1371/journal.pone.0197320. PubMed DOI PMC
Wang B, Seiler JR, Mei C. Burkholderia phytofirmans strain PsJN advanced development and altered leaf level physiology of switchgrass. Biomass Bioenergy. 2015;83:493–500. doi: 10.1016/j.biombioe.2015.10.029. DOI
Lee MR, Hawkes CV. Plant and soil drivers of whole-plant microbiomes: variation in Switchgrass Fungi from Coastal to Mountain Sites. Phytobiomes J. 2021;5(1):69–79. doi: 10.1094/pbiomes-07-20-0056-fi. DOI
Smercina DN, Evans SE, Friesen ML, Tiemann LK. Temporal dynamics of free-living nitrogen fixation in the switchgrass rhizosphere. GCB Bioenergy. 2021;13(n/a):1814–30; doi: 10.1111/gcbb.12893.
Bivand R, Keitt T, Rowlingson B. rgdal: bindings for the ‘geospatial’ data Abstraction Library. R package version 15–28. 2021.
Bivand RS, Pebesma E, Gomez-Rubio V. Applied spatial data analysis with R, second edition. NY: Springer; 2013.
Pebesma EJ, Bivand RS. Classes and methods for spatial data in R. R News. 2005;5(2):9–13.
R Core Team. : R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria; 2022.
Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, González A, Stombaugh J, et al. Moving pictures of the human microbiome. Genome Biol. 2011;12. 10.1186/gb-2011-12-5-r50. PubMed PMC
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79. 10.1128/aem.01043-13. PubMed PMC
White TJ, Bruns T, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. New York: Academic Press Inc; 1990. pp. 315–22.
Longley R, Noel ZA, Benucci GMN, Chilvers MI, Trail F, Bonito G. Crop Management Impacts the soybean (Glycine max) Microbiome. Front Microbiol. 2020;11. 10.3389/fmicb.2020.01116. PubMed PMC
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26. 10.1093/bioinformatics/btq461. PubMed
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Meth. 2013;10(10):996–8. doi: 10.1038/nmeth.2604. PubMed DOI
Edgar RC. SINTAX: a simple non-bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv. 2016;074161. 10.1101/074161.
Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “All-species living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42(Database issue):D643–D8. doi: 10.1093/nar/gkt1209. PubMed DOI PMC
Abarenkov K, Zirk A, Piirmann T, Pöhönen R, Ivanov F, Nilsson RH et al. UNITE USEARCH/UTAX release for eukaryotes. Version 04.02.2020. UNITE Community. 2020; doi: 10.15156/BIO/786376.
Saunders CW, Scheynius A, Heitman J. Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog. 2012;8(6):e1002701–e. doi: 10.1371/journal.ppat.1002701. PubMed DOI PMC
Liber JA, Bonito G, Benucci GMN. CONSTAX2: improved taxonomic classification of environmental DNA markers. Bioinformatics. 2021;37(21):3941–3. doi: 10.1093/bioinformatics/btab347. PubMed DOI
Clarke K, Gorley R, Primer . Version 6.1.10: user manual and tutorial. Plymouth: Primer-E; 2007.
Kelly BJ, Gross R, Bittinger K, Sherrill-Mix S, Lewis JD, Collman RG, et al. Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA. Bioinformatics. 2015;31(15):2461–8. doi: 10.1093/bioinformatics/btv183. PubMed DOI PMC
Gower JC. Generalized procrustes analysis. Psychometrika. 1975;40(1):33–51. doi: 10.1007/BF02291478. DOI
Lisboa FJG, Peres-Neto PR, Chaer GM, Jesus EdC, Mitchell RJ, Chapman SJ, et al. Much beyond Mantel: bringing Procrustes Association Metric to the Plant and Soil Ecologist’s Toolbox. PLoS ONE. 2014;9(6):e101238. doi: 10.1371/journal.pone.0101238. PubMed DOI PMC
Jackson DA. PROTEST: a PROcrustean randomization TEST of community environment concordance. Ecoscience. 1995;2(3):297–303. doi: 10.1080/11956860.1995.11682297. DOI
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al. vegan: Community ecology package. R package version 2.5-6. 2019.
Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models using lme4. J Stat Softw. 2015;67(1):48. doi: 10.18637/jss.v067.i01. DOI
Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest Package: Tests in Linear Mixed Effects Models. 2017. 2017;82(13):26; doi: 10.18637/jss.v082.i13.
Hartig F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. In., R package version 0.4.6 edn; 2022.
Lenth RV. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 163. 2021.
Ferrier S, Manion G, Elith J, Richardson K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers Distrib. 2007;13(3):252–64. doi: 10.1111/j.1472-4642.2007.00341.x. DOI
Fitzpatrick MC, Mokany K, Manion G, Lisk M, Ferrier S, Nieto-Lugilde D. gdm: Generalized Dissimilarity Modeling. R package version 1422. 2021.
Kassambara A. rstatix: Pipe-Friendly Framework for Basic Statistical Tests. In., R package version 0.7.0 edn; 2021.
Stekhoven DJ, Bühlmann P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics. 2011;28(1):112–8. doi: 10.1093/bioinformatics/btr597. PubMed DOI
Shade A, Stopnisek N. Abundance-occupancy distributions to prioritize plant core microbiome membership. Curr Opin Microbiol. 2019;49:50–8. doi: 10.1016/j.mib.2019.09.008. PubMed DOI
VanWallendael A, Benucci GMN, da Costa PB, Fraser L, Sreedasyam A, Fritschi F, et al. Host genotype controls ecological change in the leaf fungal microbiome. PLoS Biol. 2022;20(8):e3001681. doi: 10.1371/journal.pbio.3001681. PubMed DOI PMC
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 2016;10(3):655–64. doi: 10.1038/ismej.2015.142. PubMed DOI PMC
Foster ZSL, Sharpton TJ, Grünwald NJ, Metacoder An R package for visualization and manipulation of community taxonomic diversity data. PLoS Comput Biol. 2017;13(2):e1005404. doi: 10.1371/journal.pcbi.1005404. PubMed DOI PMC
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016;20:241–8. doi: 10.1016/j.funeco.2015.06.006. DOI
Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI et al. Endemism and functional convergence across the North American soil mycobiome. Proceedings of the National Academy of Sciences. 2014;111(17):6341-6; doi: 10.1073/pnas.1402584111. PubMed PMC
Tedersoo L, Mikryukov V, Zizka A, Bahram M, Hagh-Doust N, Anslan S, et al. Global patterns in endemicity and vulnerability of soil fungi. Glob Change Biol. 2022;28(22):6696–710. doi: 10.1111/gcb.16398. PubMed DOI PMC
Buscardo E, Geml J, Schmidt SK, Freitas H, da Cunha HB, Nagy L. Spatio-temporal dynamics of soil bacterial communities as a function of Amazon forest phenology. Sci Rep. 2018;8(1):4382. doi: 10.1038/s41598-018-22380-z. PubMed DOI PMC
Nielsen UN, Ayres E, Wall DH, Li G, Bardgett RD, Wu TH, et al. Global-scale patterns of assemblage structure of soil nematodes in relation to climate and ecosystem properties. Glob Ecol Biogeogr. 2014;23(9):968–78. doi: 10.1111/geb.12177. DOI
Phillips HRP, Guerra CA, Bartz MLC, Briones MJI, Brown G, Crowther TW, et al. Global distribution of earthworm diversity. Science. 2019;366(6464):480–5. doi: 10.1126/science.aax4851. PubMed DOI PMC
Beschoren da Costa P, Benucci GMN, Chou M-Y, Wyk JV, Chretien M, Bonito G. Soil origin and plant genotype modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly. mBio. 2022;13(2):e00079–22. doi: 10.1128/mbio.00079-22. PubMed DOI PMC
Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK. The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett. 2016;19(8):926–36. doi: 10.1111/ele.12630. PubMed DOI
Yokota M, Guan Y, Fan Y, Zhang X, Yang W. Vertical and temporal variations of soil bacterial and archaeal communities in wheat-soybean rotation agroecosystem. PeerJ. 2022;10:e12868. doi: 10.7717/peerj.12868. PubMed DOI PMC
Shen C, He J-Z, Ge Y. Seasonal dynamics of soil microbial diversity and functions along elevations across the treeline. Sci Total Environ. 2021;794:148644. doi: 10.1016/j.scitotenv.2021.148644. PubMed DOI
Landesman WJ, Freedman ZB, Nelson DM. Seasonal, sub-seasonal and diurnal variation of soil bacterial community composition in a temperate deciduous forest. FEMS Microbiol Ecol. 2019;95(2). 10.1093/femsec/fiz002. PubMed PMC
Carini P, Delgado-Baquerizo M, Hinckley E-LS, Holland-Moritz H, Brewer TE, Rue G, et al. Effects of spatial variability and Relic DNA removal on the detection of temporal Dynamics in Soil Microbial Communities. mBio. 2020;11(1):e02776–19. doi: 10.1128/mBio.02776-19. PubMed DOI PMC
Gschwend F, Hartmann M, Hug A-S, Enkerli J, Gubler A, Frey B, et al. Long-term stability of soil bacterial and fungal community structures revealed in their abundant and rare fractions. Mol Ecol. 2021;30(17):4305–20. doi: 10.1111/mec.16036. PubMed DOI PMC
Wang K, Xue K, Wang Z, Liu W, Zhao R, Wu W, et al. Accelerated temporal turnover of the soil nematode community under alpine grassland degradation. Land Degrad Dev. 2023;34(4):1171–81. doi: 10.1002/ldr.4524. DOI
Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S, et al. Seasonal variation in functional properties of microbial communities in beech forest soil. Soil Biol Biochem. 2013;60(100):95–104. doi: 10.1016/j.soilbio.2013.01.025. PubMed DOI PMC
López-Mondéjar R, Voříšková J, Větrovský T, Baldrian P. The bacterial community inhabiting temperate deciduous forests is vertically stratified and undergoes seasonal dynamics. Soil Biol Biochem. 2015;87:43–50. doi: 10.1016/j.soilbio.2015.04.008. DOI
Lladó S, Větrovský T, Baldrian P. Tracking of the activity of individual bacteria in temperate forest soils shows guild-specific responses to seasonality. Soil Biol Biochem. 2019;135:275–82. doi: 10.1016/j.soilbio.2019.05.010. DOI
Kuo H-C, Hui S, Choi J, Asiegbu FO, Valkonen JPT, Lee Y-H. Secret lifestyles of Neurospora crassa. Sci Rep. 2014;4(1):5135. doi: 10.1038/srep05135. PubMed DOI PMC
Voříšková J, Brabcová V, Cajthaml T, Baldrian P. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol. 2014;201(1):269–78. doi: 10.1111/nph.12481. PubMed DOI
Smercina DN, Evans SE, Friesen ML, Tiemann LK. Impacts of nitrogen addition on switchgrass root-associated diazotrophic community structure and function. FEMS Microbiol Ecol. 2020;96(12). 10.1093/femsec/fiaa208. PubMed
Kinoshita A, Ogura-Tsujita Y, Umata H, Sato H, Hashimoto T, Yukawa T. How do fungal partners affect the evolution and habitat preferences of mycoheterotrophic plants? A case study in Gastrodia. Am J Bot. 2016;103(2):207–20. doi: 10.3732/ajb.1500082. PubMed DOI