Paper · 2023 · The ISME Journal

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

Kai Sun; Hui-Jun Jiang; Yi-Tong Pan; et al.

7
claims
13
verbatim quotes
38
citations
1
research areas
✓
Open access

Abstract

Abstract 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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Claims 7

Observationobservedoriginal resultmeasured

Claim · model-written summary

Hyphosphere bacteria facilitated fungal hyphal spreading and root colonization in ammonium enriched soil.

Taxon
plantt0
Interactor
Phomopsis liquidambarisDiaporthe liquidambarise0symbiont
Outcome
hyphal spreading and assist in the root colonizatione0
Setting
NH4+-enriched soile0

Verbatim

e0

“Phomopsis liquidambaris, harbors specific hyphosphere bacteria that facilitate hyphal spreading and assist in the root colonization in NH4+-enriched soil.”

✓ located verbatim in the source · abstract, characters 488–642 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Enterobacter was enriched around the sensitive wild type relative to the deficient strain.

Taxon
plantt0
Interactor
EnterobacterEnterobactere0symbiont
Outcome
Enterobacter was enrichede0
Direction
enrichede0
Comparator
NH4+-preferring nitrite reductase-deficient straine0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Enterobacter
Enterobacter · Interactor · picture of the genus (one of its species)Public domain · Wikimedia Commons ↗

Verbatim

e0

“Enterobacter was enriched in the hyphosphere of NH4+-sensitive wild-type compared to NH4+-preferring nitrite reductase-deficient strain.”

✓ located verbatim in the source · abstract, characters 737–873 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

SZ2 promoted fungal hyphal spreading only in nonsterilized soil.

Taxon
plantt0
Interactor
Enterobacter sp. SZ2e0symbiont
Outcome
hyphal spreadinge0
Setting
nonsterilized soile0

Verbatim

e0

“Enterobacter sp. SZ2-promoted hyphal spreading is only evident in nonsterilized soil.”

✓ located verbatim in the source · abstract, characters 893–978 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

SZ2 inoculation increased abundance and diversity of ammonia oxidizing archaea.

Taxon
plantt0
Interactor
ammonia-oxidizing archaea (AOA)Nitrososphaerotae0symbiont
Outcome
abundance and diversity of ammonia-oxidizing archaea (AOA)e0
Direction
increasede0

Verbatim

e0

“increased abundance and diversity of ammonia-oxidizing archaea (AOA) and a synchronously decreased NH4+:NO3− ratio following SZ2 inoculation.”

✓ located verbatim in the source · abstract, characters 1004–1145 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

SZ2 inoculation decreased the soil ammonium to nitrate ratio.

Taxon
plantt0
Interactor
SZ2e0symbiont
Outcome
NH4+:NO3− ratioe0
Direction
decreasede0

Verbatim

e0

“a synchronously decreased NH4+:NO3− ratio following SZ2 inoculation.”

✓ located verbatim in the source · abstract, characters 1077–1145 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

AOA mediated ratio reduction explained improved fungal adaptation.

Taxon
plantt0
Interactor
AOANitrososphaerotae0symbiont
Outcome
fungal adaptation to NH4+-enriched conditionse0

Verbatim

e0

“AOA-mediated reduction in NH4+:NO3− ratio is responsible for SZ2-enhanced fungal adaptation to NH4+-enriched conditions.”

✓ located verbatim in the source · abstract, characters 1205–1325 · show in text ↑
t0

“plant”

✓ located verbatim in the source · title, characters 80–85 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The fungal bacterial archaeal interaction promoted rice growth under ammonium enrichment.

Treatment
Ph. liquidambaris-Enterobacter-AOA triple interactione0
Interactor
Ph. liquidambarise0symbiont
Outcome
rice growthe0
Direction
promotede0
Setting
NH4+-enriched soile0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH4+-enriched soil.”

✓ located verbatim in the source · abstract, characters 1326–1427 · show in text ↑

Enterobacter · growth · Oryza sativa (rice)Results differ

4 papers: 3 positive, 1 negative or no effect

2 papers in the same direction as this paper · 1 in the opposite direction

  1. negative
  2. positive
  3. positive
See all 4 papers →

ph · growth · Oryza sativa (rice)Positive and negative results

26 papers: 11 positive, 15 negative or no effect

10 papers in the same direction as this paper · 15 in the opposite direction

  1. negative
  2. negative
  3. negative

22 papers more in this group

See all 26 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.