Hyphosphere Microorganisms Facilitate Hyphal Spreading and Root Colonization of Plant Symbiotic Fungus in Ammonium-enriched Soil

Overview

Journal ISME J

Publisher Oxford University Press

Specialties Environmental Health
Microbiology

Date 2023 Jul 13

PMID 37443341

Authors

Kai Sun

Hui-Jun Jiang

Yi-Tong Pan

Fan Lu

Qiang Zhu

Chen-Yu Ma

Ai-Yue Zhang

Jia-Yu Zhou

Wei Zhang

Chuan-Chao Dai

Affiliations

Soon will be listed here.

Abstract

Anthropogenic nitrogen inputs lead to a high ammonium (NH)/nitrate (NO) ratio in the soil, which restricts hyphal spreading of soil fungi. Access of symbiotic fungi to roots is a prerequisite for plant-fungal interactions. Hyphosphere bacteria protect fungi from environmental stress, yet the impact of hyphosphere bacteria on adaptation of host fungi to NH-enriched conditions remains unclear. By developing soil microcosm assays, we report that a plant-symbiotic fungus, Phomopsis liquidambaris, harbors specific hyphosphere bacteria that facilitate hyphal spreading and assist in the root colonization in NH-enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH-sensitive wild-type compared to NH-preferring nitrite reductase-deficient strain. The representative Enterobacter sp. SZ2-promoted hyphal spreading is only evident in nonsterilized soil. We further identified an increased abundance and diversity of ammonia-oxidizing archaea (AOA) and a synchronously decreased NH:NO ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH:NO ratio is responsible for SZ2-enhanced fungal adaptation to NH-enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH-enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems.

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References

Guether M, Balestrini R, Hannah M, He J, Udvardi M, Bonfante P . Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol. 2009; 182(1):200-212. DOI: 10.1111/j.1469-8137.2008.02725.x. View

Peng L, Shan X, Yang Y, Wang Y, Druzhinina I, Pan X . Facultative symbiosis with a saprotrophic soil fungus promotes potassium uptake in American sweetgum trees. Plant Cell Environ. 2021; 44(8):2793-2809. DOI: 10.1111/pce.14053. View

Hiruma K, Gerlach N, Sacristan S, Nakano R, Hacquard S, Kracher B . Root Endophyte Colletotrichum tofieldiae Confers Plant Fitness Benefits that Are Phosphate Status Dependent. Cell. 2016; 165(2):464-74. PMC: 4826447. DOI: 10.1016/j.cell.2016.02.028. View

Sui X, Zhang T, Tian Y, Xue R, Li A . A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic Pedicularis species. New Phytol. 2018; 221(1):470-481. DOI: 10.1111/nph.15379. View

Buttner H, Niehs S, Vandelannoote K, Cseresnyes Z, Dose B, Richter I . Bacterial endosymbionts protect beneficial soil fungus from nematode attack. Proc Natl Acad Sci U S A. 2021; 118(37. PMC: 8449335. DOI: 10.1073/pnas.2110669118. View

Dahlstrom K, Newman D . Soil bacteria protect fungi from phenazines by acting as toxin sponges. Curr Biol. 2021; 32(2):275-288.e5. PMC: 8792240. DOI: 10.1016/j.cub.2021.11.002. View

Rozmos M, Bukovska P, Hrselova H, Kotianova M, Dudas M, Gancarcikova K . Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist. ISME J. 2021; 16(3):676-685. PMC: 8857242. DOI: 10.1038/s41396-021-01112-8. View

Zhang L, Zhou J, George T, Limpens E, Feng G . Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends Plant Sci. 2021; 27(4):402-411. DOI: 10.1016/j.tplants.2021.10.008. View

Nguyen N . Fungal Hyphosphere Microbiomes Are Distinct from Surrounding Substrates and Show Consistent Association Patterns. Microbiol Spectr. 2023; :e0470822. PMC: 10100729. DOI: 10.1128/spectrum.04708-22. View

10.

Emmett B, Levesque-Tremblay V, Harrison M . Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 2021; 15(8):2276-2288. PMC: 8319317. DOI: 10.1038/s41396-021-00920-2. View

11.

Luthfiana N, Inamura N, Tantriani , Sato T, Saito K, Oikawa A . Metabolite profiling of the hyphal exudates of Rhizophagus clarus and Rhizophagus irregularis under phosphorus deficiency. Mycorrhiza. 2021; 31(3):403-412. DOI: 10.1007/s00572-020-01016-z. View

12.

Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S . Bacterial-fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev. 2018; 42(3):335-352. DOI: 10.1093/femsre/fuy008. View

13.

Jiang F, Zhang L, Zhou J, George T, Feng G . Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 2020; 230(1):304-315. DOI: 10.1111/nph.17081. View

14.

Otto S, Bruni E, Harms H, Wick L . Catch me if you can: dispersal and foraging of Bdellovibrio bacteriovorus 109J along mycelia. ISME J. 2016; 11(2):386-393. PMC: 5270576. DOI: 10.1038/ismej.2016.135. View

15.

Junier P, Cailleau G, Palmieri I, Vallotton C, Trautschold O, Junier T . Democratization of fungal highway columns as a tool to investigate bacteria associated with soil fungi. FEMS Microbiol Ecol. 2021; 97(2). PMC: 7878174. DOI: 10.1093/femsec/fiab003. View

16.

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(3):1022-32. DOI: 10.1111/nph.13838. View

17.

Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P . Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J. 2015; 10(1):130-44. PMC: 4681866. DOI: 10.1038/ismej.2015.91. View

18.

Mondo S, Lastovetsky O, Gaspar M, Schwardt N, Barber C, Riley R . Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi. Nat Commun. 2017; 8(1):1843. PMC: 5705715. DOI: 10.1038/s41467-017-02052-8. View

19.

Torres-Cortes G, Ghignone S, Bonfante P, Schussler A . Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association. Proc Natl Acad Sci U S A. 2015; 112(25):7785-90. PMC: 4485150. DOI: 10.1073/pnas.1501540112. View

20.

Desiro A, Hao Z, Liber J, Benucci G, Lowry D, Roberson R . Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle. ISME J. 2018; 12(7):1743-1757. PMC: 6018737. DOI: 10.1038/s41396-018-0053-9. View