Fungal Hyphosphere Microbiomes Are Distinct from Surrounding Substrates and Show Consistent Association Patterns

Nguyen, Nhu

doi:10.1128/spectrum.04708-22

Cited by 7 publications

(1 citation statement)

References 83 publications

(109 reference statements)

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“…The exceptions are Devosia and Microvirga (Order Hyphomicrobiales), which we were not able to isolate, perhaps due to their low level of occurrence. The occurrence of Cupriavidus and other rhizobia such as Mesorhizobium in the rhizosphere of many non-legume plant hosts and fungal-rich habitats suggests that they have an external "free living" phase in the rhizosphere where they consume root and fungal exudates [36][37][38], and a more well-known symbiotic phase inside of nodules. A much more detailed sampling and species-level identification these rhizobia strains will be required to confirm these associations.…”

Section: Discussionmentioning

confidence: 99%

Legume-nodulating rhizobia are widespread in soils and plants across the island of O‘ahu, Hawai‘i

Abe,

Dhungana,

Nguyen

2023

PLoS ONE

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Legumes and their interaction with rhizobia represent one of the most well-characterized symbioses that are widespread across both natural and agricultural environments. However, larger distribution patterns and host associations on isolated Pacific islands with many native and introduced hosts have not been well-documented. Here, we used molecular and culturing techniques to characterize rhizobia from soils and 24 native and introduced legume species on the island of O’ahu, Hawai‘i. We chose two of these isolates to inoculate an endemic legume tree, Erythina sandwicensis to measure nodulation potentials and host benefits. We found that all rhizobia genera can be found in the soil, where only Cupriavidus was found at all sites, although at lower abundance relative to other more common genera such as Rhizobium (and close relatives), Bradyzhizobium, and Devosia. Bradyrhizobium was the most common nodulator of legumes, where the strain Bradyrhizobium sp. strain JA1 is a generalist capable of forming nodules on nine different host species, including two native species. In greenhouse nursery inoculations, the two different Bradyrhizobium strains successfully nodulate the endemic E. sandwicensis; both strains equally and significantly increased seedling biomass in nursery inoculations. Overall, this work provides a molecular-based framework in which to study potential native and introduced rhizobia on one of the most isolated archipelagos on the planet.

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Section: Discussionmentioning

confidence: 99%

Legume-nodulating rhizobia are widespread in soils and plants across the island of O‘ahu, Hawai‘i

Abe,

Dhungana,

Nguyen

2023

PLoS ONE

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Soil microbial holobiont interplay and its role in protecting plants against salinity stress

SLITI,

SINGH,

PANDE

et al. 2024

Pedosphere

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Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil

et al. 2023

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Anthropogenic nitrogen inputs lead to a high ammonium (NH4+)/nitrate (NO3−) 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 NH4+-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 NH4+-enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH4+-sensitive wild-type compared to NH4+-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 NH4+:NO3− ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH4+:NO3− ratio is responsible for SZ2-enhanced fungal adaptation to NH4+-enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH4+-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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Fungal Hyphosphere Microbiomes Are Distinct from Surrounding Substrates and Show Consistent Association Patterns

Cited by 7 publications

References 83 publications

Legume-nodulating rhizobia are widespread in soils and plants across the island of O‘ahu, Hawai‘i

Legume-nodulating rhizobia are widespread in soils and plants across the island of O‘ahu, Hawai‘i

Soil microbial holobiont interplay and its role in protecting plants against salinity stress

Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil

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