A tripartite bacterial-fungal-plant symbiosis in the mycorrhiza-shaped microbiome drives plant growth and mycorrhization.
Arbuscular mycorrhiza fungi
Mycorrhization
Nitrogen uptake
Organic farming
Plant growth
Plant microbiome
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
19 Jan 2024
19 Jan 2024
Historique:
received:
19
07
2023
accepted:
18
11
2023
medline:
22
1
2024
pubmed:
20
1
2024
entrez:
19
1
2024
Statut:
epublish
Résumé
Plant microbiomes play crucial roles in nutrient cycling and plant growth, and are shaped by a complex interplay between plants, microbes, and the environment. The role of bacteria as mediators of the 400-million-year-old partnership between the majority of land plants and, arbuscular mycorrhizal (AM) fungi is still poorly understood. Here, we test whether AM hyphae-associated bacteria influence the success of the AM symbiosis. Using partitioned microcosms containing field soil, we discovered that AM hyphae and roots selectively assemble their own microbiome from the surrounding soil. In two independent experiments, we identified several bacterial genera, including Devosia, that are consistently enriched on AM hyphae. Subsequently, we isolated 144 pure bacterial isolates from a mycorrhiza-rich sample of extraradical hyphae and isolated Devosia sp. ZB163 as root and hyphal colonizer. We show that this AM-associated bacterium synergistically acts with mycorrhiza on the plant root to strongly promote plant growth, nitrogen uptake, and mycorrhization. Our results highlight that AM fungi do not function in isolation and that the plant-mycorrhiza symbiont can recruit beneficial bacteria that support the symbiosis. Video Abstract.
Sections du résumé
BACKGROUND
BACKGROUND
Plant microbiomes play crucial roles in nutrient cycling and plant growth, and are shaped by a complex interplay between plants, microbes, and the environment. The role of bacteria as mediators of the 400-million-year-old partnership between the majority of land plants and, arbuscular mycorrhizal (AM) fungi is still poorly understood. Here, we test whether AM hyphae-associated bacteria influence the success of the AM symbiosis.
RESULTS
RESULTS
Using partitioned microcosms containing field soil, we discovered that AM hyphae and roots selectively assemble their own microbiome from the surrounding soil. In two independent experiments, we identified several bacterial genera, including Devosia, that are consistently enriched on AM hyphae. Subsequently, we isolated 144 pure bacterial isolates from a mycorrhiza-rich sample of extraradical hyphae and isolated Devosia sp. ZB163 as root and hyphal colonizer. We show that this AM-associated bacterium synergistically acts with mycorrhiza on the plant root to strongly promote plant growth, nitrogen uptake, and mycorrhization.
CONCLUSIONS
CONCLUSIONS
Our results highlight that AM fungi do not function in isolation and that the plant-mycorrhiza symbiont can recruit beneficial bacteria that support the symbiosis. Video Abstract.
Identifiants
pubmed: 38243337
doi: 10.1186/s40168-023-01726-4
pii: 10.1186/s40168-023-01726-4
pmc: PMC10799531
doi:
Substances chimiques
Soil
0
Types de publication
Video-Audio Media
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
13Subventions
Organisme : Swiss National Science Foundation
ID : grant 310030-188799
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : grant 310030-188799
Pays : Switzerland
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2024. The Author(s).
Références
Strullu-Derrien C, Selosse MA, Kenrick P, Martin FM. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol. 2018;220:1012–30.
pubmed: 29573278
doi: 10.1111/nph.15076
Brundrett M. Diversity and classification of mycorrhizal associations. Biol Rev. 2004;79:473–95.
pubmed: 15366760
doi: 10.1017/S1464793103006316
Chowdhury S, Lange M, Malik AA, Goodall T, Huang J, Griffiths RI, Gleixner G. Plants with arbuscular mycorrhizal fungi efficiently acquire Nitrogen from substrate additions by shaping the decomposer community composition and their net plant carbon demand. Plant Soil. 2022;475:473–90.
doi: 10.1007/s11104-022-05380-x
Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, Veen JAv, Kowalchuk GA. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO
pubmed: 20534474
pmcid: 2890735
doi: 10.1073/pnas.0912421107
Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature. 2005;435:819–23.
pubmed: 15944705
doi: 10.1038/nature03610
Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK. An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol. 2013;15:1870–81.
pubmed: 23360621
doi: 10.1111/1462-2920.12081
Pfeffer PE, Douds DD Jr, Bécard G, Shachar-Hill Y. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 1999;120:587–98.
pubmed: 10364411
pmcid: 59298
doi: 10.1104/pp.120.2.587
Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol. 2016;210:1022–32.
pubmed: 27074400
doi: 10.1111/nph.13838
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 2015;205:1406–23.
pubmed: 25639293
doi: 10.1111/nph.13288
Cosme M. Mycorrhizas drive the evolution of plant adaptation to drought. Commun Biol. 2023;6:346.
pubmed: 36997637
pmcid: 10063553
doi: 10.1038/s42003-023-04722-4
Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
pubmed: 22564542
doi: 10.1016/j.tplants.2012.04.001
Zhang L, Zhou J, George TS, Limpens E, Feng G. Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends plant sci. 2021;27(4):402–11.
pubmed: 34782247
doi: 10.1016/j.tplants.2021.10.008
Pieterse CMJ, de Jonge R, Berendsen RL. The soil-borne supremacy. Trends Plant Sci. 2016;21:171–3.
pubmed: 26853594
doi: 10.1016/j.tplants.2016.01.018
Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018;23:25–41.
pubmed: 29050989
doi: 10.1016/j.tplants.2017.09.003
Cosme M, Fernández I, Declerck S, van der Heijden MGA, Pieterse CMJ. A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana. Plant Mol Biol. 2021;106:319–34.
pubmed: 33825084
doi: 10.1007/s11103-021-01143-x
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD. Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol. 2007;61:295–304.
pubmed: 17535297
doi: 10.1111/j.1574-6941.2007.00337.x
Filion M, St-Arnaud M, Fortin J. Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol. 1999;141:525–33.
doi: 10.1046/j.1469-8137.1999.00366.x
Hartman K, Schmid MW, Bodenhausen N, Bender SF, Valzano-Held AY, Schlaeppi K, van der Heijden MGA. A symbiotic footprint in the plant root microbiome. Environ Microbiome. 2023;18(1):65.
pubmed: 37525294
pmcid: 10391997
doi: 10.1186/s40793-023-00521-w
Linderman R. Mycorrhizal interactions in the rhizosphere. In The Rhizosphere and Plant Growth: Papers presented at a Symposium held May 8–11, 1989, at the Beltsville Agricultural Research Center (BARC). Maryland: Springer; 1991. p. 343–8.
doi: 10.1007/978-94-011-3336-4_73
Scheublin TR, Sanders IR, Keel C, Van Der Meer JR. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. 2010;4:752–63.
pubmed: 20147983
doi: 10.1038/ismej.2010.5
Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD. Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett. 2006;254:34–40.
pubmed: 16451176
doi: 10.1111/j.1574-6968.2005.00003.x
Emmett BD, Lévesque-Tremblay V, Harrison MJ. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 2021;15:2276–88.
pubmed: 33649552
pmcid: 8319317
doi: 10.1038/s41396-021-00920-2
Zhang L, Shi N, Fan J, Wang F, George TS, Feng G. Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environ Microbiol. 2018;20:2639–51.
pubmed: 29901256
doi: 10.1111/1462-2920.14289
Nuccio EE, Blazewicz SJ, Lafler M, Campbell AN, Kakouridis A, Kimbrel JA, Wollard J, Vyshenska D, Riley R, Tomatsu A. HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi. Microbiome. 2022;10:1–20.
doi: 10.1186/s40168-022-01391-z
Li X, Zhao R, Li D, Wang G, Bei S, Ju X, An R, Li L, Kuyper TW, Christie P, et al. Mycorrhiza-mediated recruitment of complete denitrifying Pseudomonas reduces N2O emissions from soil. Microbiome. 2023;11:45.
pubmed: 36890606
pmcid: 9996866
doi: 10.1186/s40168-023-01466-5
Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 2018;12:1296–307.
pubmed: 29382946
pmcid: 5931975
doi: 10.1038/s41396-018-0059-3
Frey-Klett P, Garbaye J, Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol. 2007;176:22–36.
pubmed: 17803639
doi: 10.1111/j.1469-8137.2007.02191.x
Roesti D, Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M. Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol. 2005;71:6673–9.
pubmed: 16269696
pmcid: 1287740
doi: 10.1128/AEM.71.11.6673-6679.2005
Xavier LJC, Germida JJ. Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem. 2003;35:471–8.
doi: 10.1016/S0038-0717(03)00003-8
Toro M, Azcon R, Barea J. Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability ((sup32)P) and nutrient cycling. Appl Environ Microbiol. 1997;63:4408–12.
pubmed: 16535730
pmcid: 1389286
doi: 10.1128/aem.63.11.4408-4412.1997
Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C. Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol. 2010;11:97–105.
doi: 10.1016/j.baae.2009.12.001
Thiele-Bruhn S, Bloem J, de Vries FT, Kalbitz K, Wagg C. Linking soil biodiversity and agricultural soil management. Current Opinion in Environmental Sustainability. 2012;4:523–8.
doi: 10.1016/j.cosust.2012.06.004
Hole DG, Perkins AJ, Wilson JD, Alexander IH, Grice PV, Evans AD. Does organic farming benefit biodiversity? Biol Cons. 2005;122:113–30.
doi: 10.1016/j.biocon.2004.07.018
Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, Keller T, Charles R, van der Heijden MGA. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019;13:1722–36.
pubmed: 30850707
pmcid: 6591126
doi: 10.1038/s41396-019-0383-2
Wittwer RA, Franz Bender S, Hartman K, Hydbom S, Lima RAA, Loaiza V, Nemecek T, Oehl F, Axel Olsson P, Petchey O, et al. Organic and conservation agriculture promote ecosystem multifunctionality. Science Advance. 2021;7:6995.
Hartman K, van der Heijden MGA, Wittwer RA, Banerjee S, Walser JC, Schlaeppi K. Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome. 2018;6:14.
pubmed: 29338764
pmcid: 5771023
doi: 10.1186/s40168-017-0389-9
Cáceres MD, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566–74.
pubmed: 20120823
doi: 10.1890/08-1823.1
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (Lf) Druce. Appl Environ Microbiol. 2002;68:5217–22.
pubmed: 12406707
pmcid: 129907
doi: 10.1128/AEM.68.11.5217-5222.2002
George E, Marschner H, Jakobsen I. Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit Rev Biotechnol. 1995;15:257–70.
doi: 10.3109/07388559509147412
Stämmler F, Gläsner J, Hiergeist A, Holler E, Weber D, Oefner PJ, Gessner A, Spang R. Adjusting microbiome profiles for differences in microbial load by spike-in bacteria. Microbiome. 2016;4:28.
pubmed: 27329048
pmcid: 4915049
doi: 10.1186/s40168-016-0175-0
Masterson RV, Prakash RK, Atherly AG. Conservation of symbiotic nitrogen fixation gene sequences in Rhizobium japonicum and Bradyrhizobium japonicum. J Bacteriol. 1985;163:21–6.
pubmed: 4008441
pmcid: 219075
doi: 10.1128/jb.163.1.21-26.1985
Roberts GP, MacNeil T, MacNeil D, Brill WJ. Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae. J Bacteriol. 1978;136:267–79.
pubmed: 361694
pmcid: 218657
doi: 10.1128/jb.136.1.267-279.1978
Schlüter J-P, Reinkensmeier J, Daschkey S, Evguenieva-Hackenberg E, Janssen S, Jänicke S, Becker JD, Giegerich R, Becker A. A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti. BMC Genomics. 2010;11:1–35.
doi: 10.1186/1471-2164-11-245
Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics. 2012;13:1–12.
Lin F, Wu Y, Ding Z, Zhou Z, Lin X, Majrashi A, Eissa MA, Ali EF. Effect of two urea forms and organic fertilizer derived from expired milk products on dynamic of NH
doi: 10.3390/agronomy11061113
Chhetri G, Kim I, Kang M, Kim J, So Y, Seo T. Devosia rhizoryzae sp. nov., and Devosia oryziradicis sp. nov., novel plant growth promoting members of the genus Devosia, isolated from the rhizosphere of rice plants. J Microbiol. 2022;60:1–10.
pubmed: 34826099
doi: 10.1007/s12275-022-1474-8
Amoo AE, Babalola OO. Ammonia-oxidizing microorganisms: key players in the promotion of plant growth. J Soil Sci Plant Nutr. 2017;17:935–47.
doi: 10.4067/S0718-95162017000400008
Jakobsen I, Rosendahl L. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 1990;115:77–83.
doi: 10.1111/j.1469-8137.1990.tb00924.x
Pearson JN, Jakobsenf I. Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New PhytoL. 1993;124:481–8.
doi: 10.1111/j.1469-8137.1993.tb03839.x
Wang L, Zhang L, George TS, Feng G. A core microbiome in the hyphosphere of arbuscular mycorrhizal fungi has functional significance in organic phosphorus mineralization. New Phytol. 2023;238:859–73.
pubmed: 36444521
doi: 10.1111/nph.18642
Petters S, Groß V, Söllinger A, Pichler M, Reinhard A, Bengtsson MM, Urich T. The soil microbial food web revisited: predatory myxobacteria as keystone taxa? ISME J. 2021;15:2665–75.
pubmed: 33746204
pmcid: 8397742
doi: 10.1038/s41396-021-00958-2
Lévesque V, Rochette P, Hogue R, Jeanne T, Ziadi N, Chantigny MH, Dorais M, Antoun H. Greenhouse gas emissions and soil bacterial community as affected by biochar amendments after periodic mineral fertilizer applications. Biol Fertil Soils. 2020;56:907–25.
doi: 10.1007/s00374-020-01470-z
Uddin M, Chen J, Qiao X, Tian R, Arafat Y, Yang X. Bacterial community variations in paddy soils induced by application of veterinary antibiotics in plant-soil systems. Ecotoxicol Environ Saf. 2019;167:44–53.
pubmed: 30292975
doi: 10.1016/j.ecoenv.2018.09.101
Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q. Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils. 2012;48:807–16.
doi: 10.1007/s00374-012-0675-4
Vosátka M, Gryndler M. Treatment with culture fractions from Pseudomonas putida modifies the development of Glomus fistulosum mycorrhiza and the response of potato and maize plants to inoculation. Appl Soil Ecol. 1999;11:245–51.
doi: 10.1016/S0929-1393(98)00151-6
Cosme M, Wurst S. Interactions between arbuscular mycorrhizal fungi, rhizobacteria, soil phosphorus and plant cytokinin deficiency change the root morphology, yield and quality of tobacco. Soil Biol Biochem. 2013;57:436–43.
doi: 10.1016/j.soilbio.2012.09.024
Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY. Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol. 2005;39:4640–6.
pubmed: 16047804
doi: 10.1021/es047979z
Liou JSC, Madsen EL. Microbial ecological processes: aerobic/anaerobic. Encyclopedia Ecol. 2008;1:2348–57.
Leghari SJ, Wahocho NA, Laghari GM, HafeezLaghari A, MustafaBhabhan G, HussainTalpur K, Bhutto TA, Wahocho SA, Lashari AA. Role of nitrogen for plant growth and development: a review. Adv Environ Biol. 2016;10:209–19.
Smith SE, Read DJ. Mycorrhizal symbiosis. Cambridge: Academic press; 2010.
Smith SE, Smith FA. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol. 2011;62:227–50.
pubmed: 21391813
doi: 10.1146/annurev-arplant-042110-103846
López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N. GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol. 2006;43:102–10.
pubmed: 16386437
doi: 10.1016/j.fgb.2005.10.005
Desiro A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P. Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME J. 2014;8:257–70.
pubmed: 24008325
doi: 10.1038/ismej.2013.151
Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC. Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol. 2000;46:229–36.
pubmed: 10749536
doi: 10.1139/w99-137
Vierheilig H, Coughlan AP, Wyss U, Piché Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol. 1998;64:5004–7.
pubmed: 9835596
pmcid: 90956
doi: 10.1128/AEM.64.12.5004-5007.1998
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol. 1990;115:495–501.
pubmed: 33874272
doi: 10.1111/j.1469-8137.1990.tb00476.x
Pacioni G. 16 Wet-sieving and decanting techniques for the extraction of spores of vesicular-arbuscular fungi. Methods Microbiol. 1992;24:317–22.
doi: 10.1016/S0580-9517(08)70099-0
Wagg C, Bender SF, Widmer F, Van Der Heijden MGA. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA. 2014;111:5266–70.
pubmed: 24639507
pmcid: 3986181
doi: 10.1073/pnas.1320054111
Herlemann DPR, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011;5:1571–9.
pubmed: 21472016
pmcid: 3176514
doi: 10.1038/ismej.2011.41
Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG. Strong succession in arbuscular mycorrhizal fungal communities. ISME J. 2019;13:214–26.
pubmed: 30171254
doi: 10.1038/s41396-018-0264-0
Taylor DL, Walters WA, Lennon NJ, Bochicchio J, Krohn A, Caporaso JG, Pennanen T. Accurate estimation of fungal diversity and abundance through improved lineage-specific primers optimized for Illumina amplicon sequencing. Appl Environ Microbiol. 2016;82:7217–26.
pubmed: 27736792
pmcid: 5118932
doi: 10.1128/AEM.02576-16
Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 2008;74:2461–70.
pubmed: 18296538
pmcid: 2293150
doi: 10.1128/AEM.02272-07
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547.
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613.
pubmed: 28005526
pmcid: 5563544
doi: 10.1099/ijsem.0.001755
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: A versatile open source tool for metagenomics. PeerJ. 2016;2016:e2584–e2584.
doi: 10.7717/peerj.2584
Fortin JA, Bécard G, Declerck S, Dalpé Y, St-Arnaud M, Coughlan AP, Piché Y. Arbuscular mycorrhiza on root-organ cultures. Can J Bot. 2002;80:1–20.
doi: 10.1139/b01-139
Murphy J, Riley JP. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta. 1962;27:31–6.
doi: 10.1016/S0003-2670(00)88444-5
Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM, Kishony R. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS ONE. 2015;10:e0128036.
pubmed: 26000737
pmcid: 4441430
doi: 10.1371/journal.pone.0128036
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
pubmed: 23193283
doi: 10.1093/nar/gks1219
Gaio D, Anantanawat K, To J, Liu M, Monahan L, Darling AE. Hackflex: Low-cost, high-throughput, Illumina Nextera Flex library construction. Microb Genom. 2022;8:000744.
pubmed: 35014949
pmcid: 8914357
Coil D, Jospin G, Darling AE. A5-miseq: An updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015;31:587–9.
pubmed: 25338718
doi: 10.1093/bioinformatics/btu661
Prokka ST. Rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.
doi: 10.1093/bioinformatics/btu153
Aziz RK, Bartels D, Best A, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, et al. The RAST Server: Rapid annotations using subsystems technology. BMC Genomics. 2008;9:75.
pubmed: 18261238
pmcid: 2265698
doi: 10.1186/1471-2164-9-75
Heller P, Tripp HJ, Turk-Kubo K, Zehr JP. ARBitrator: a software pipeline for on-demand retrieval of auto-curated nifH sequences from GenBank. Bioinformatics. 2014;30:2883–90.
pubmed: 24990605
doi: 10.1093/bioinformatics/btu417
Moynihan MA. nifHdada2 GitHub repository. Zenodo. 2020. https://doi.org/10.5281/zenodo.3958370 .
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal. 2011;17:10–2.
doi: 10.14806/ej.17.1.200
Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F. Improved software detection and extraction of ITS1 and ITS 2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol. 2013;4:914–9.
doi: 10.1111/2041-210X.12073
Werner JJ, Koren O, Hugenholtz P, Desantis TZ, Walters WA, Caporaso JG, Angenent LT, Knight R, Ley RE. Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J. 2012;6:94–103 Nature Publishing Group;
pubmed: 21716311
doi: 10.1038/ismej.2011.82
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–7.
pubmed: 24112409
doi: 10.1111/mec.12481
R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2018. Retrieved from https://www.R-project.or .
Bisanz JE. qiime2R: Importing QIIME2 artifacts and associated data into R sessions. Version. 2018;099:13.
McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.
pubmed: 23630581
pmcid: 3632530
doi: 10.1371/journal.pone.0061217
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR. O’hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. Community ecology package R package version. 2013;2:321–6.
Wickham, H, Winston C. "Package ‘ggplot2’." Create elegant data visualisations using the grammar of graphics. Version 2.1. 2016. p. 1–189.
Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32:2847–9.
pubmed: 27207943
doi: 10.1093/bioinformatics/btw313