Abstract
The extraradical hyphae-associated microbiome of arbuscular mycorrhizal fungi (AMF), the “hyphosphere microbiome,” harbors a diverse reservoir of microbes. The biological interactions in the AMF hyphosphere have major implications for soil carbon and nutrient cycling, soil food web dynamics, and plant nutrition and health. Hyphosphere microbial communities are thought to assist AMF in accessing organic nutrients by degrading complex organic compounds that AMF are unable to do by themselves. The AMF, in return, provide an energy-rich microhabitat supplied with hyphal exudates that facilitates microbial growth and mobility in the hyphosphere. However, our current knowledge of hyphosphere entities, their trophic interactions and functional roles, and the underlying mechanisms facilitating microbial co-occurrence and co-operation is largely incomplete. Here, we review the current state of knowledge on the identity and putative roles of AMF hyphae-associated microbes, with a specific focus on prokaryotes, and potential drivers of such microbial communities in the hyphosphere. Moreover, we discuss the knowledge gaps and open challenges that should be addressed and prioritized in future studies on the AMF microbiomes. We also provide an appraisal of available and emerging tools and technologies and highlight the need for innovative approaches to disentangle AMF hyphosphere processes and answer the many unresolved questions.
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Abeysinghe G, Kuchira M, Kudo G, Masuo S, Ninomiya A, Takahashi K, Utada AS, Hagiwara D, Nomura N, Takaya N, Obana N, Takeshita N (2020) Fungal mycelia and bacterial thiamine establish a mutualistic growth mechanism. Life Sci Alliance 3:e202000878. https://doi.org/10.26508/lsa.202000878
Adeyemi NO, Atayese MO, Sakariyawo OS, Azeez JO, AbayomiSobowale SP, Olubode A, Mudathir R, Adebayo R, Adeoye S (2021) Alleviation of heavy metal stress by arbuscular mycorrhizal symbiosis in Glycine max (L.) grown in copper, lead and zinc contaminated soils. Rhizosphere 18:100325. https://doi.org/10.1016/j.rhisph.2021.100325
Agnolucci M, Battini F, Cristani C, Giovannetti M (2015) Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fertil Soils 51:379–389. https://doi.org/10.1007/s00374-014-0989-5
Aleklett K, Kiers ET, Ohlsson P, Shimizu TS, Caldas VEA, Hammer EC (2018) Build your own soil: exploring microfluidics to create microbial habitat structures. Isme J 12:312–319. https://doi.org/10.1038/ismej.2017.184
Aleklett K, Ohlsson P, Bengtsson M, Hammer EC (2021) Fungal foraging behaviour and hyphal space exploration in micro-structured Soil Chips. Isme J 15:1782–1793. https://doi.org/10.1038/s41396-020-00886-7
Alteio LV, Séneca J, Canarini A, Angel R, Jansa J, Guseva K, Kaiser C, Richter A, Schmidt H (2021) A critical perspective on interpreting amplicon sequencing data in soil ecological research. Soil Biol Biochem 160:108357. https://doi.org/10.1016/j.soilbio.2021.108357
Amaro F, Martín-González A (2021) Microbial warfare in the wild—the impact of protists on the evolution and virulence of bacterial pathogens. Int Microbiol 24:559–571. https://doi.org/10.1007/s10123-021-00192-y
Amaro F, Wang W, Gilbert JA, Roger Anderson O, Shuman HA (2015) Diverse protist grazers select for virulence-related traits in Legionella. Isme J 9:1607–1618. https://doi.org/10.1038/ismej.2014.248
Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192:71–79. https://doi.org/10.1023/a:1004249629643
Arellano-Caicedo C, Ohlsson P, Bengtsson M, Beech JP, Hammer EC (2021) Habitat geometry in artificial microstructure affects bacterial and fungal growth, interactions, and substrate degradation. Commun Biol 4:1226. https://doi.org/10.1038/s42003-021-02736-4
Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215. https://doi.org/10.1128/AEM.69.10.6208-6215.2003
Artursson V, Finlay RD, Jansson JK (2005) Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol 7:1952–1966. https://doi.org/10.1111/j.1462-2920.2005.00868.x
Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10. https://doi.org/10.1111/j.1462-2920.2005.00942.x
Bakker P, Berendsen R, Doornbos R, Wintermans P, Pieterse C (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165. https://doi.org/10.3389/fpls.2013.00165
Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010. https://doi.org/10.1128/aem.62.8.3005-3010.1996
Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol Plant Microbe in 14:255–260. https://doi.org/10.1094/MPMI.2001.14.2.255
Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504
Bonfante P, Balestrini R, Mend Gen K (1994) Storage and secretion processes in the spore of Gigaspora margarita Becker and Hall as revealed by high-pressure freezing and freeze substitution. New Phytol 128:93–101. https://doi.org/10.1111/j.1469-8137.1994.tb03991.x
Bonfante P, Venice F, Lanfranco L (2019) The mycobiota: fungi take their place between plants and bacteria. Curr Opin Microbiol 49:18–25. https://doi.org/10.1016/j.mib.2019.08.004
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631. https://doi.org/10.1111/j.1469-8137.2004.01066.x
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
Bukovská P, Gryndler M, Gryndlerová H, Püschel D, Jansa J (2016) Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. Front Microbiol 7:711. https://doi.org/10.3389/fmicb.2016.00711
Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, Řezáčová V, Gutiérrez-Núñez MS, Gryndler M, Jansa J (2018) Utilization of organic nitrogen by arbuscular mycorrhizal fungi-is there a specific role for protists and ammonia oxidizers? Mycorrhiza 28:465–465. https://doi.org/10.1007/s00572-018-0851-y
Bukovská P, Rozmoš M, Kotianová M, Gančarčíková K, Dudáš M, Hršelová H, Jansa J (2021) Arbuscular mycorrhiza mediates efficient recycling from soil to plants of nitrogen bound in chitin. Front Microbiol 12:325. https://doi.org/10.3389/fmicb.2021.574060
Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP (2019) Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? Isme J 13:1891–1898. https://doi.org/10.1038/s41396-019-0403-2
Cruz-Paredes C, Diera T, Davey M, Rieckmann MM, Christensen P, Dela Cruz M, Laursen KH, Joner EJ, Christensen JH, Nybroe O, Jakobsen I (2021) Disentangling the abiotic and biotic components of AMF suppressive soils. Soil Biol Biochem 159:108305. https://doi.org/10.1016/j.soilbio.2021.108305
de Boer W (2017) Upscaling of fungal–bacterial interactions: from the lab to the field. Curr Opin Microbiol 37:35–41. https://doi.org/10.1016/j.mib.2017.03.007
de Novais CB, Sbrana C, da Conceição JE, Rouws LFM, Giovannetti M, Avio L, Siqueira JO, Saggin Júnior OJ, da Silva EMR, de Faria SM (2020) Mycorrhizal networks facilitate the colonization of legume roots by a symbiotic nitrogen-fixing bacterium. Mycorrhiza 30:389–396. https://doi.org/10.1007/s00572-020-00948-w
Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P (2014) Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. Isme J 8:257–270. https://doi.org/10.1038/ismej.2013.151
Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky OA, Mieszkin S, Millet LJ, Vajna B, Junier P, Bonfante P, Krom BP, Olsson S, van Elsas JD, Wick LY (2018) Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev 42:335–352. https://doi.org/10.1093/femsre/fuy008
Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HT, Bodelier PL, Whiteley AS, Van Veen JA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. P Natl Acad Sci USA 107:10938–10942. https://doi.org/10.1073/pnas.0912421107
Dudáš M, Pjevac P, Kotianová M, Gančarčíková K, Rozmoš M, Hršelová H, Bukovská P, Jansa J (2022) Arbuscular mycorrhiza and nitrification: disentangling processes and players through using synthetic nitrification inhibitors. Appl Environ Microbiol 88:20. https://doi.org/10.1128/aem.01369-22
Dumont MG, Hernández García M (2019) Stable isotope probing, methods and protocols Humana Press, New York, USA. 247
Ehlers K, Bünemann EK, Oberson A, Frossard E, Frostegård Å, Yuejian M, Bakken LR (2008) Extraction of soil bacteria from a Ferralsol. Soil Biol Biochem 40:1940–1946. https://doi.org/10.1016/j.soilbio.2008.04.005
Emmett BD, Lévesque-Tremblay V, Harrison MJ (2021) Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. Isme J 15:2276–2288. https://doi.org/10.1038/s41396-021-00920-2
Etesami H, Jeong BR, Glick BR (2021) Contribution of arbuscular mycorrhizal fungi, phosphate–solubilizing bacteria, and silicon to P uptake by plant. Front Plant Sci 12:1355. https://doi.org/10.3389/fpls.2021.69961
Faghihinia M, Zou Y, Chen Z, Bai Y, Li W, Marrs R, Staddon PL (2020) The response of grassland mycorrhizal fungal abundance to a range of long-term grazing intensities. Rhizosphere 13:100178. https://doi.org/10.1016/j.rhisph.2019.100178
Fortin JA, Bécard G, Declerck S, Dalpé Y, St-Arnaud M, Coughlan AP, Piché Y (2002) Arbuscular mycorrhiza on root-organ cultures. Can J Bot 80:1–20. https://doi.org/10.1139/b01-139
Gahan J, Schmalenberger A (2015) Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization. Appl Soil Ecol 89:113–121. https://doi.org/10.1016/j.apsoil.2014.12.008
Gao X, Guo H, Zhang Q, Guo H, Zhang L, Zhang C, Gou Z, Liu Y, Wei J, Chen A, Chu Z, Zeng F (2020) Arbuscular mycorrhizal fungi (AMF) enhanced the growth, yield, fiber quality and phosphorus regulation in upland cotton (Gossypium hirsutum L.). Sci Rep 10:2084. https://doi.org/10.1038/s41598-020-59180-3
Gao D, Pan X, Khashi u Rahman M, Zhou X, Wu F (2021) Common mycorrhizal networks benefit to the asymmetric interspecific facilitation via K exchange in an agricultural intercropping system. Biol Fertil Soils 57:959–971. https://doi.org/10.1007/s00374-021-01561-5
Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24. https://doi.org/10.1007/s11104-005-3701-6
Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M, Schweiger P, Eichorst SA, Wagner M, Richter A, Schintlmeister A, Woebken D, Kaiser C (2019) Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability. Front Microbiol 10:168. https://doi.org/10.3389/fmicb.2019.00168
Gryndler M, Hršelová H, Stříteská D (2000) Effect of soil bacteria on hyphal growth of the arbuscular mycorrhizal fungus Glomus claroideum. Folia Microbiol 45:545–551. https://doi.org/10.1007/BF02818724
Gryndler M, Šmilauer P, Püschel D, Bukovská P, Hršelová H, Hujslová M, Gryndlerová H, Beskid O, Konvalinková T, Jansa J (2018) Appropriate nonmycorrhizal controls in arbuscular mycorrhiza research: a microbiome perspective. Mycorrhiza 28:435–450. https://doi.org/10.1007/s00572-018-0844-x
Henkes GJ, Kandeler E, Marhan S, Scheu S, Bonkowski M (2018) Interactions of mycorrhiza and protists in the rhizosphere systemically alter microbial community composition, plant shoot-to-root ratio and within-root system nitrogen allocation. Front Environ Sci 6:117. https://doi.org/10.3389/fenvs.2018.00117
Hestrin R, Kan MG, Lafler M, Wollard J, Kimbrel JA, Ray P, Blazewicz SJ, Stuart R, Craven K, Firestone M, Nuccio EE, Pett-Ridge J (2022) Plant-associated fungi support bacterial resilience following water limitation. Isme J Press. https://doi.org/10.1038/s41396-022-01308-6
Hildebrandt U, Janetta K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919–1924. https://doi.org/10.1128/AEM.68.4.1919-1924.2002
Holátko J, Brtnický M, Kučerík J, Kotianová M, Elbl J, Kintl A, Kynický J, Benada O, Datta R, Jansa J (2021) Glomalin – truths, myths, and the future of this elusive soil glycoprotein. Soil Biol Biochem 153:108116. https://doi.org/10.1016/j.soilbio.2020.108116
Huang X, Li Y, Liu B, Guggenberger G, Shibistova O, Zhu Z, Ge T, Tan W, Wu J (2017) SoilChip-XPS integrated technique to study formation of soil biogeochemical interfaces. Soil Biol Biochem 113:71–79. https://doi.org/10.1016/j.soilbio.2017.05.021
Hünninghaus M, Dibbern D, Kramer S, Koller R, Pausch J, Schloter-Hai B, Urich T, Kandeler E, Bonkowski M, Lueders T (2019) Disentangling carbon flow across microbial kingdoms in the rhizosphere of maize. Soil Biol Biochem 134:122–130. https://doi.org/10.1016/j.soilbio.2019.03.007
Jansa J, Hodge A (2021) Swimming, gliding, or hyphal riding? On microbial migration along the arbuscular mycorrhizal hyphal highway and functional consequences thereof. New Phytol 230:14–16. https://doi.org/10.1111/nph.17244
Jansa J, Treseder K (2017) Introduction: Mycorrhizas and the carbon cycle. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal mediation of soil: fertility, structure and carbon storage. Elsevier, Amsterdam, pp 343–355
Jiang Y, Luan L, Hu K, Liu M, Chen Z, Geisen S, Chen X, Li H, Xu Q, Bonkowski M, Sun B (2020) Trophic interactions as determinants of the arbuscular mycorrhizal fungal community with cascading plant-promoting consequences. Microbiome 8:142. https://doi.org/10.1186/s40168-020-00918-6
Jiang F, Zhang L, Zhou JC, George TS, Feng G (2021) Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol 230:304–315. https://doi.org/10.1111/nph.17081
Junier P, Cailleau G, Palmieri I, Vallotton C, Trautschold OC, Junier T, Paul C, Bregnard D, Palmieri F, Estoppey A, Buffi M, Lohberger A, Robinson A, Kelliher JM, Davenport K, House GL, Morales D, Gallegos-Graves LV, Dichosa AEK, Lupini S, Nguyen HN, Young JD, Rodrigues DF, Parra-Vasquez ANG, Bindschedler S, Chain PSG (2021) Democratization of fungal highway columns as a tool to investigate bacteria associated with soil fungi. FEMS Microbiol Rev 97:fiab003. https://doi.org/10.1093/femsec/fiab003
Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551. https://doi.org/10.1111/nph.13138
Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T (2016) Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211:1202–1208. https://doi.org/10.1111/nph.14016
Kohlmeier S, Smits TH, Ford RM, Keel C, Harms H, Wick LY, technology (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci 39:4640–4646. https://doi.org/10.1021/es047979z
Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517. https://doi.org/10.1046/j.1469-8137.2000.00776.x
Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211. https://doi.org/10.1111/nph.12249
Koller R, Scheu S, Bonkowski M, Robin C (2013) Protozoa stimulate N uptake and growth of arbuscular mycorrhizal plants. Soil Biol Biochem 65:204–210. https://doi.org/10.1016/j.soilbio.2013.05.020
Kubota K, Morono Y, Ito M, Terada T, Itezono S, Harada H, Inagaki F (2014) Gold-ISH: a nano-size gold particle-based phylogenetic identification compatible with NanoSIMS. Syst Appl Microbiol 37:261–266. https://doi.org/10.1016/j.syapm.2014.02.003
Linderman R (1991) The rhizosphere and plant growth. In: Keister D.L., P.B. C (eds), Beltsville Symposia in Agricultural Research, p. 343–348. Springer, Dordrecht, The Netherlands
Liu P, Pommerenke B, Conrad R (2018) Identification of Syntrophobacteraceae as major acetate-degrading sulfate reducing bacteria in Italian paddy soil. Environ Microbiol 20:337–354. https://doi.org/10.1111/1462-2920.14001
Liu S, Zhang X, Dungait JAJ, Quine TA, Razavi BS (2021) Rare microbial taxa rather than phoD gene abundance determine hotspots of alkaline phosphomonoesterase activity in the karst rhizosphere soil. Biol Fertil Soils 57:257–268. https://doi.org/10.1007/s00374-020-01522-4
Luthfiana N, Inamura N, Tantriani ST, Saito K, Oikawa A, Chen W, Tawaraya K (2021) Metabolite profiling of the hyphal exudates of Rhizophagus clarus and Rhizophagus irregularis under phosphorus deficiency. Mycorrhiza 31:403–412. https://doi.org/10.1007/s00572-020-01016-z
Mafla-Endara PM, Arellano-Caicedo C, Aleklett K, Pucetaite M, Ohlsson P, Hammer EC (2021) Microfluidic chips provide visual access to in situ soil ecology. Commun Biol 4:1–12. https://doi.org/10.1038/s42003-021-02379-5
Marschner H (1995) Mineral nutrition of higher plants, 2nd ed. Academic Press London. 889
Massalha H, Korenblum E, Malitsky S, Shapiro OH, Aharoni A (2017) Live imaging of root–bacteria interactions in a microfluidics setup. P Natl Acad Sci USA 114:4549–4554. https://doi.org/10.1073/pnas.1618584114
Mayali X, Weber PK (2018) Quantitative isotope incorporation reveals substrate partitioning in a coastal microbial community. FEMS Microbiol Ecol 94 https://doi.org/10.1093/femsec/fiy047
Mayerhofer W, Schintlmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, Gabriel R, Reipert S, Weidinger M, Clode P, Wagner M, Woebken D, Richter A, Kaiser C (2021) Recently photoassimilated carbon and fungus-delivered nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica. New Phytol 232:2457–2474. https://doi.org/10.1111/nph.17591
Messa VR, Savioli MR (2021) Improving sustainable agriculture with arbuscular mycorrhizae. Rhizosphere 19:100412. https://doi.org/10.1016/j.rhisph.2021.100412
Musat N, Musat F, Weber PK, Pett-Ridge J (2016) Tracking microbial interactions with NanoSIMS. Curr Opin Microbiol 41:114–121. https://doi.org/10.1016/j.copbio.2016.06.007
Nazir R, Tazetdinova DI, van Elsas JD (2014) Burkholderia terrae BS001 migrates proficiently with diverse fungal hosts through soil and provides protection from antifungal agents. Front Microbiol 5:598. https://doi.org/10.3389/fmicb.2014.00598
Noirot-Gros M-F, Shinde SV, Akins C, Johnson JL, Zerbs S, Wilton R, Kemner KM, Noirot P, Babnigg G (2020) Functional imaging of microbial interactions with tree roots using a microfluidics setup. Front Plant Sci 11:408. https://doi.org/10.3389/fpls.2020.00408
Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881. https://doi.org/10.1111/1462-2920.12081
Nuccio EE, Blazewicz SJ, Lafler M, Campbell AN, Kakouridis A, Kimbrel JA, Wollard J, Vyshenska D, Riley R, Tomatsu A, Hestrin R, Malmstrom RR, Firestone M, Pett-Ridge J (2022) HT-SIP: a semi-automated Stable Isotope Probing pipeline identifies interactions in the hyphosphere of arbuscular mycorrhizal fungi. BioRxiv preprint. https://doi.org/10.1101/2022.07.01.498377
Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Moot D, Ryan MH (2017) Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. Mycorrhiza 27:619–638. https://doi.org/10.1007/s00572-017-0782-z
Otto S, Bruni EP, Harms H, Wick LY (2017) Catch me if you can: dispersal and foraging of Bdellovibrio bacteriovorus 109J along mycelia. Isme J 11:386–393. https://doi.org/10.1038/ismej.2016.135
Pett-Ridge J, Firestone M (2017) Using stable isotopes to explore root-microbe-mineral interactions in soil. Rhizosphere 3:244–253. https://doi.org/10.1016/j.rhisph.2017.04.016
Pivato B, Offre P, Marchelli S, Barbonaglia B, Mougel C, Lemanceau P, Berta G (2009) Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19:81–90. https://doi.org/10.1007/s00572-008-0205-2
Poveda J, Hermosa R, Monte E, Nicolás C (2019) Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Sci Rep 9:11650. https://doi.org/10.1038/s41598-019-48269-z
Pucetaite M, Ohlsson P, Persson P, Hammer E (2021) Shining new light into soil systems: spectroscopy in microfluidic soil chips reveals microbial biogeochemistry. Soil Biol Biochem 153:108078. https://doi.org/10.1016/j.soilbio.2020.108078
Purin S, Rillig MC (2008) Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence. FEMS Microbiol Lett 279:8–14. https://doi.org/10.1111/j.1574-6968.2007.01007.x
Püschel D, Bitterlich M, Rydlová J, Jansa J (2021) Drought accentuates the role of mycorrhiza in phosphorus uptake. Soil Biol Biochem 157:108243. https://doi.org/10.1016/j.soilbio.2021.108243
Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403:646–649. https://doi.org/10.1038/35001054
Ray P, Lakshmanan V, Labbé JL, Craven KD (2020) Microbe to microbiome: a paradigm shift in the application of microorganisms for sustainable agriculture. Front Microbiol 11:3323. https://doi.org/10.3389/fmicb.2020.622926
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. P Natl Acad Sci USA 91:11841–11843. https://doi.org/10.1073/pnas.91.25.11841
Rozmoš M, Bukovská P, Hršelová H, Kotianová M, Dudáš M, Gančarčíková K, Jansa J (2022) Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist. Isme J 16:676–685. https://doi.org/10.1038/s41396-021-01112-8
Rubin BE, Diamond S, Cress BF, Crits-Christoph A, Lou YC, Borges AL, Shivram H, He C, Xu M, Zhou Z, Smith SJ, Rovinsky R, Smock DCJ, Tang K, Owens TK, Krishnappa N, Sachdeva R, Barrangou R, Deutschbauer AM, Banfield JF, Doudna JA (2022) Species- and site-specific genome editing in complex bacterial communities. Nat Microbiol 7:34–47. https://doi.org/10.1038/s41564-021-01014-7
Rubinstein RL, Kadilak AL, Cousens VC, Gage DJ, Shor LM (2015) Protist-facilitated particle transport using emulated soil micromodels. Environ Sci Technol 49:1384–1391. https://doi.org/10.1021/es503424z
Scheublin TR, Sanders IR, Keel C, van der Meer JR (2010) Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. Isme J 4:752–763. https://doi.org/10.1038/ismej.2010.5
Schwarz A, Adetutu EM, Juhasz AL, Aburto-Medina A, Ball AS, Shahsavari E (2018) Microbial degradation of phenanthrene in pristine and contaminated sandy soils. Microb Ecol 75:888–902. https://doi.org/10.1007/s00248-017-1094-8
Šimek K, Vrba J, Pernthaler J, Posch T, Hartman P, Nedoma J, Psenner R (1997) Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl Environ Microbiol 63:587–595. https://doi.org/10.1128/aem.63.2.587-595.1997
Sinanaj B, Hoysted GA, Pressel S, Bidartondo MI, Field KJ (2021) Critical research challenges facing Mucoromycotina ‘fine root endophytes.’ New Phytol 232:1528–1534. https://doi.org/10.1111/nph.17684
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, San Diego CA, USA, p 787
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042
Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I (2018) Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. Isme J 12:1296–1307. https://doi.org/10.1038/s41396-018-0059-3
Talbot J, Allison S, Treseder K (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963. https://doi.org/10.1111/j.1365-2435.2008.01402.x
Tamayo E, Gómez-Gallego T, Azcón-Aguilar C, Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:547. https://doi.org/10.3389/fpls.2014.00547
Thirkell TJ, Cameron DD, Hodge A (2016) Resolving the ‘nitrogen paradox’ of arbuscular mycorrhizas: fertilization with organic matter brings considerable benefits for plant nutrition and growth. Plant Cell Environ 39:1683–1690. https://doi.org/10.1111/pce.12667
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, dit Frey NF, Gianinazzi-Pearson V (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. P Natl Acad Sci USA 110:20117–20122. https://doi.org/10.1073/pnas.1313452110
Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254:34–40. https://doi.org/10.1111/j.1574-6968.2005.00003.x
Tourlousse DM, Yoshiike S, Ohashi A, Matsukura S, Noda N, Sekiguchi Y (2017) Synthetic spike-in standards for high-throughput 16S rRNA gene amplicon sequencing. Nucleic Acids Res 45:e23. https://doi.org/10.1093/nar/gkw984
Treseder KK, Cross A (2006) Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9:305–316. https://doi.org/10.1007/s10021-005-0110-x
Tringe SG (2022) A toolkit for microbial community editing. Nat Rev Microbiol 20:383. https://doi.org/10.1038/s41579-022-00747-4
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288
Veresoglou SD, Verbruggen E, Makarova O, Mansour I, Sen R, Rillig MC (2019) Arbuscular mycorrhizal fungi alter the community structure of ammonia oxidizers at high fertility via competition for soil NH4. Microb Ecol 78:147–158. https://doi.org/10.1007/s00248-018-1281-2
Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797. https://doi.org/10.1104/pp.112.195727
Wang F, Shi N, Jiang RF, Zhang FS, Feng G (2016) In situ stable isotope probing of phosphate-solubilizing bacteria in the hyphosphere. J Exp Bot 67:1689–1701. https://doi.org/10.1093/jxb/erv561
Wang F, Kertesz MA, Feng G (2019) Phosphorus forms affect the hyphosphere bacterial community involved in soil organic phosphorus turnover. Mycorrhiza 29:351–362. https://doi.org/10.1007/s00572-019-00896-0
Wang F, Zhang L, Zhou J, Rengel Z, George TS, Feng G (2022) Exploring the secrets of hyphosphere of arbuscular mycorrhizal fungi: processes and ecological functions. Plant Soil Press. https://doi.org/10.1007/s11104-022-05621-z
Wei X, Hu Y, Razavi BS, Zhou J, Shen J, Nannipieri P, Wu J, Ge T (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70. https://doi.org/10.1016/j.soilbio.2018.12.025
Weremijewicz J, Janos DP (2013) Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol 198:203–213. https://doi.org/10.1111/nph.12125
Wick LY, Remer R, Würz B, Reichenbach J, Braun S, Schäfer F, Harms H (2007) Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environ Sci 41:500–505. https://doi.org/10.1021/es061407s
Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478. https://doi.org/10.1016/S0038-0717(03)00003-8
Zai X-M, Fan J-J, Hao Z-P, Liu X-M, Zhang W-X (2021) Effect of co-inoculation with arbuscular mycorrhizal fungi and phosphate solubilizing fungi on nutrient uptake and photosynthesis of beach palm under salt stress environment. Sci Rep 11:5761. https://doi.org/10.1038/s41598-021-84284-9
Zhang L, Fan JQ, Ding XD, He XH, Zhang FS, Feng G (2014) Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biol Biochem 74:177–183. https://doi.org/10.1016/j.soilbio.2014.03.004
Zhang L, Xu MG, Liu Y, Zhang FS, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032. https://doi.org/10.1111/nph.13838
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. Isme J 12:2339–2351. https://doi.org/10.1038/s41396-018-0171-4
Zhang L, Shi N, Fan JQ, Wang F, George TS, Feng G (2018) Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environ Microbiol 20:2639–2651. https://doi.org/10.1111/1462-2920.14289
Zhang L, Peng Y, Zhou JC, George TS, Feng G (2020) Addition of fructose to the maize hyphosphere increases phosphatase activity by changing bacterial community structure. Soil Biol Biochem 142:107724. https://doi.org/10.1016/j.soilbio.2020.107724
Zhang L, Zhou J, George TS, Limpens E, Feng G (2022) Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends Plant Sci 27:402–411. https://doi.org/10.1016/j.tplants.2021.10.008
Zhou JC, Chai XF, Zhang L, George TS, Wang F, Feng G (2020) Different arbuscular mycorrhizal fungi cocolonizing on a single plant root system recruit distinct microbiomes. mSystems 5:e00929-00920. https://doi.org/10.1128/mSystems.00929-20
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This work was supported by The Ministry of Education, Youth and Sports of Czech Republic (CZ.02.2.69/0.0/0.0/18_053/0017705), Czech Academy of Sciences (RVO 61388971), and Grant Agency of the Czech Republic (21-07275S).
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Faghihinia and Jansa conceived and developed the review. Faghihinia drafted the first version of the manuscript. Faghihinia, Jansa, Halverson, and Staddon contributed to revisions and all approved the final version.
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Faghihinia, M., Jansa, J., Halverson, L.J. et al. Hyphosphere microbiome of arbuscular mycorrhizal fungi: a realm of unknowns. Biol Fertil Soils 59, 17–34 (2023). https://doi.org/10.1007/s00374-022-01683-4
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DOI: https://doi.org/10.1007/s00374-022-01683-4