Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly

Ke Tao; Ib T Jensen; Sha Zhang; Eber Villa-Rodríguez; Zuzana Blahovska; Camilla Lind Salomonsen; Anna Martyn; Þuríður Nótt Björgvinsdóttir; Simon Kelly; Luc Janss; Marianne Glasius; Rasmus Waagepetersen; Simona Radutoiu

doi:10.1038/s41467-024-47752-0

Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly

Ke Tao, Ib T Jensen, Sha Zhang, Eber Villa-Rodríguez, Zuzana Blahovska, Camilla Lind Salomonsen, Anna Martyn, Þuríður Nótt Björgvinsdóttir, Simon Kelly, Luc Janss, Marianne Glasius, Rasmus Waagepetersen, Simona Radutoiu^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Symbiosis with soil-dwelling bacteria that fix atmospheric nitrogen allows legume plants to grow in nitrogen-depleted soil. Symbiosis impacts the assembly of root microbiota, but it is unknown how the interaction between the legume host and rhizobia impacts the remaining microbiota and whether it depends on nitrogen nutrition. Here, we use plant and bacterial mutants to address the role of Nod factor signaling on Lotus japonicus root microbiota assembly. We find that Nod factors are produced by symbionts to activate Nod factor signaling in the host and that this modulates the root exudate profile and the assembly of a symbiotic root microbiota. Lotus plants with different symbiotic abilities, grown in unfertilized or nitrate-supplemented soils, display three nitrogen-dependent nutritional states: starved, symbiotic, or inorganic. We find that root and rhizosphere microbiomes associated with these states differ in composition and connectivity, demonstrating that symbiosis and inorganic nitrogen impact the legume root microbiota differently. Finally, we demonstrate that selected bacterial genera characterizing state-dependent microbiomes have a high level of accurate prediction.

Original language	English
Article number	3436
Journal	Nature Communications
Volume	15
Issue	1
Number of pages	15
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-024-47752-0
Publication status	Published - Apr 2024

Keywords

Lotus/microbiology
Symbiosis
Nitrogen/metabolism
Plant Roots/microbiology
Signal Transduction
Microbiota/physiology
Rhizosphere
Bacterial Proteins/metabolism
Soil Microbiology
Nitrogen Fixation
Plant Exudates/metabolism

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Tao, K., Jensen, I. T., Zhang, S., Villa-Rodríguez, E., Blahovska, Z., Salomonsen, C. L., Martyn, A., Björgvinsdóttir, Þ. N., Kelly, S., Janss, L., Glasius, M., Waagepetersen, R., & Radutoiu, S. (2024). Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly. Nature Communications, 15(1), Article 3436. https://doi.org/10.1038/s41467-024-47752-0

@article{80ac6d47dcd040a690e75af870769e91,

title = "Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly",

abstract = "Symbiosis with soil-dwelling bacteria that fix atmospheric nitrogen allows legume plants to grow in nitrogen-depleted soil. Symbiosis impacts the assembly of root microbiota, but it is unknown how the interaction between the legume host and rhizobia impacts the remaining microbiota and whether it depends on nitrogen nutrition. Here, we use plant and bacterial mutants to address the role of Nod factor signaling on Lotus japonicus root microbiota assembly. We find that Nod factors are produced by symbionts to activate Nod factor signaling in the host and that this modulates the root exudate profile and the assembly of a symbiotic root microbiota. Lotus plants with different symbiotic abilities, grown in unfertilized or nitrate-supplemented soils, display three nitrogen-dependent nutritional states: starved, symbiotic, or inorganic. We find that root and rhizosphere microbiomes associated with these states differ in composition and connectivity, demonstrating that symbiosis and inorganic nitrogen impact the legume root microbiota differently. Finally, we demonstrate that selected bacterial genera characterizing state-dependent microbiomes have a high level of accurate prediction.",

keywords = "Lotus/microbiology, Symbiosis, Nitrogen/metabolism, Plant Roots/microbiology, Signal Transduction, Microbiota/physiology, Rhizosphere, Bacterial Proteins/metabolism, Soil Microbiology, Nitrogen Fixation, Plant Exudates/metabolism",

author = "Ke Tao and Jensen, {Ib T} and Sha Zhang and Eber Villa-Rodr{\'i}guez and Zuzana Blahovska and Salomonsen, {Camilla Lind} and Anna Martyn and Bj{\"o}rgvinsd{\'o}ttir, {{\TH}ur{\'i}{\dh}ur N{\'o}tt} and Simon Kelly and Luc Janss and Marianne Glasius and Rasmus Waagepetersen and Simona Radutoiu",

note = "{\textcopyright} 2024. The Author(s).",

year = "2024",

month = apr,

doi = "10.1038/s41467-024-47752-0",

language = "English",

volume = "15",

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Tao, K, Jensen, IT, Zhang, S , Villa-Rodríguez, E , Blahovska, Z , Salomonsen, CL, Martyn, A, Björgvinsdóttir, ÞN, Kelly, S, Janss, L , Glasius, M, Waagepetersen, R & Radutoiu, S 2024, 'Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly', Nature Communications, vol. 15, no. 1, 3436. https://doi.org/10.1038/s41467-024-47752-0

TY - JOUR

T1 - Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly

AU - Tao, Ke

AU - Jensen, Ib T

AU - Zhang, Sha

AU - Villa-Rodríguez, Eber

AU - Blahovska, Zuzana

AU - Salomonsen, Camilla Lind

AU - Martyn, Anna

AU - Björgvinsdóttir, Þuríður Nótt

AU - Kelly, Simon

AU - Janss, Luc

AU - Glasius, Marianne

AU - Waagepetersen, Rasmus

AU - Radutoiu, Simona

PY - 2024/4

Y1 - 2024/4

N2 - Symbiosis with soil-dwelling bacteria that fix atmospheric nitrogen allows legume plants to grow in nitrogen-depleted soil. Symbiosis impacts the assembly of root microbiota, but it is unknown how the interaction between the legume host and rhizobia impacts the remaining microbiota and whether it depends on nitrogen nutrition. Here, we use plant and bacterial mutants to address the role of Nod factor signaling on Lotus japonicus root microbiota assembly. We find that Nod factors are produced by symbionts to activate Nod factor signaling in the host and that this modulates the root exudate profile and the assembly of a symbiotic root microbiota. Lotus plants with different symbiotic abilities, grown in unfertilized or nitrate-supplemented soils, display three nitrogen-dependent nutritional states: starved, symbiotic, or inorganic. We find that root and rhizosphere microbiomes associated with these states differ in composition and connectivity, demonstrating that symbiosis and inorganic nitrogen impact the legume root microbiota differently. Finally, we demonstrate that selected bacterial genera characterizing state-dependent microbiomes have a high level of accurate prediction.

AB - Symbiosis with soil-dwelling bacteria that fix atmospheric nitrogen allows legume plants to grow in nitrogen-depleted soil. Symbiosis impacts the assembly of root microbiota, but it is unknown how the interaction between the legume host and rhizobia impacts the remaining microbiota and whether it depends on nitrogen nutrition. Here, we use plant and bacterial mutants to address the role of Nod factor signaling on Lotus japonicus root microbiota assembly. We find that Nod factors are produced by symbionts to activate Nod factor signaling in the host and that this modulates the root exudate profile and the assembly of a symbiotic root microbiota. Lotus plants with different symbiotic abilities, grown in unfertilized or nitrate-supplemented soils, display three nitrogen-dependent nutritional states: starved, symbiotic, or inorganic. We find that root and rhizosphere microbiomes associated with these states differ in composition and connectivity, demonstrating that symbiosis and inorganic nitrogen impact the legume root microbiota differently. Finally, we demonstrate that selected bacterial genera characterizing state-dependent microbiomes have a high level of accurate prediction.

KW - Lotus/microbiology

KW - Symbiosis

KW - Nitrogen/metabolism

KW - Plant Roots/microbiology

KW - Signal Transduction

KW - Microbiota/physiology

KW - Rhizosphere

KW - Bacterial Proteins/metabolism

KW - Soil Microbiology

KW - Nitrogen Fixation

KW - Plant Exudates/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85191050470&partnerID=8YFLogxK

U2 - 10.1038/s41467-024-47752-0

DO - 10.1038/s41467-024-47752-0

M3 - Journal article

C2 - 38653767

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3436

ER -

Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly

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Keywords

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