Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants

Senga Robertson; Alexandros Mosca; Saira Ashraf; Aileen Corral; Rodrigo Alegria Terrazas; Catherine Arnton; Peter Thorpe; Jenny A. Morris; Pete E. Hedley; Giulia Babbi; Castrense  Savojardo; Pier Luigi Martelli; Frederik Duus Møller; Hanne Nørgaard Nielsen; Pimlapas Leekitcharoenphon; Frank M. Aarestrup; Rashi Halder; Cedric C. Laczny; Paul Wilmes; Laura Pietrantonio; Pardo Di Cillo; Vittoria Catara; James Abbott; Davide Bulgarelli

doi:10.1128/msphere.00842-25

Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants

Senga Robertson
, Alexandros Mosca
, Saira Ashraf
, Aileen Corral
, Rodrigo Alegria Terrazas
, Catherine Arnton
, Peter Thorpe
, Jenny A. Morris
, Pete E. Hedley
, Giulia Babbi
, Castrense Savojardo
, Pier Luigi Martelli
, Frederik Duus Møller
, Hanne Nørgaard Nielsen
, Pimlapas Leekitcharoenphon
, Frank M. Aarestrup
, Rashi Halder
, Cedric C. Laczny
, Paul Wilmes
, Laura Pietrantonio

Pardo Di Cillo, Vittoria Catara, James Abbott, Davide Bulgarelli (Lead / Corresponding author)

Research output: Contribution to journal › Article › peer-review

Abstract

Tomato is a staple crop and an excellent model to study host-microbiota interactions in the plant food chain. In this study, we describe a “lab-in-the-field” approach to investigate the microbiota of field-grown tomato plants. High-throughput amplicon sequencing revealed a three-microhabitat partition, phyllosphere, rhizosphere, and root interior, differentiating host-associated communities from the environmental microbiota. An individual bacterium, classified as Acinetobacter sp., emerged as a dominant member of the microbiota at the plant-soil continuum. To gain insights into the functional significance of this enrichment, we subjected rhizosphere specimens to shotgun metagenomics. Similar to the amplicon sequencing survey, a “microhabitat effect,” defined by a set of rhizosphere-enriched functions, was identified. Mobilization of mineral nutrients, as well as adaptation to salinity and polymicrobial communities, including antimicrobial resistance genes (ARGs), emerged as a functional requirement sustaining metagenomic diversification. A metagenome-assembled genome representative of Acinetobacter calcoaceticus was retrieved, and metagenomic reads associated with this species identified a functional specialization for plant-growth promotion traits, such as phosphate solubilization, siderophore production, and reactive oxygen species detoxification, which were similarly represented in a tomato genotype-independent fashion. Our results revealed that the enrichment of a beneficial bacterium capable of alleviating plant abiotic stresses appears decoupled from ARGs facilitating microbiota persistence at the root-soil interface.

Original language	English
Article number	e00842-25
Number of pages	21
Journal	mSphere
Early online date	15 Jan 2026
DOIs	https://doi.org/10.1128/msphere.00842-25
Publication status	E-pub ahead of print - 15 Jan 2026

Keywords

food-chain microbiota
tomato
metagenomics
AMR
One Health

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10.1128/msphere.00842-25Licence: CC BY

Final Published VersionFinal published version, 1.54 MBLicence: CC BY

Controlling mIcRobiomes CircuLations for bEtter food Systems (CIRCLES) (joint with Alma Mater Studiorum - Universita di Bologna as lead, PanepistimioThessalias, Bolton Alimentari and 26 others)
Bulgarelli, D. (Investigator)
COMMISSION OF THE EUROPEAN COMMUNITIES
1/11/18 → 31/10/24
Project: Research

Cite this

Robertson, S., Mosca, A., Ashraf, S., Corral, A., Alegria Terrazas, R., Arnton, C., Thorpe, P., Morris, J. A., Hedley, P. E., Babbi, G., Savojardo, C., Martelli, P. L., Møller, F. D., Nielsen, H. N., Leekitcharoenphon, P., Aarestrup, F. M., Halder, R., Laczny, C. C., Wilmes, P., ... Bulgarelli, D. (2026). Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants. mSphere, Article e00842-25. Advance online publication. https://doi.org/10.1128/msphere.00842-25

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title = "Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants",

abstract = "Tomato is a staple crop and an excellent model to study host-microbiota interactions in the plant food chain. In this study, we describe a “lab-in-the-field” approach to investigate the microbiota of field-grown tomato plants. High-throughput amplicon sequencing revealed a three-microhabitat partition, phyllosphere, rhizosphere, and root interior, differentiating host-associated communities from the environmental microbiota. An individual bacterium, classified as Acinetobacter sp., emerged as a dominant member of the microbiota at the plant-soil continuum. To gain insights into the functional significance of this enrichment, we subjected rhizosphere specimens to shotgun metagenomics. Similar to the amplicon sequencing survey, a “microhabitat effect,” defined by a set of rhizosphere-enriched functions, was identified. Mobilization of mineral nutrients, as well as adaptation to salinity and polymicrobial communities, including antimicrobial resistance genes (ARGs), emerged as a functional requirement sustaining metagenomic diversification. A metagenome-assembled genome representative of Acinetobacter calcoaceticus was retrieved, and metagenomic reads associated with this species identified a functional specialization for plant-growth promotion traits, such as phosphate solubilization, siderophore production, and reactive oxygen species detoxification, which were similarly represented in a tomato genotype-independent fashion. Our results revealed that the enrichment of a beneficial bacterium capable of alleviating plant abiotic stresses appears decoupled from ARGs facilitating microbiota persistence at the root-soil interface.",

keywords = "food-chain microbiota, tomato, metagenomics, AMR, One Health",

author = "Senga Robertson and Alexandros Mosca and Saira Ashraf and Aileen Corral and \{Alegria Terrazas\}, Rodrigo and Catherine Arnton and Peter Thorpe and Morris, \{Jenny A.\} and Hedley, \{Pete E.\} and Giulia Babbi and Castrense Savojardo and Martelli, \{Pier Luigi\} and M{\o}ller, \{Frederik Duus\} and Nielsen, \{Hanne N{\o}rgaard\} and Pimlapas Leekitcharoenphon and Aarestrup, \{Frank M.\} and Rashi Halder and Laczny, \{Cedric C.\} and Paul Wilmes and Laura Pietrantonio and \{Di Cillo\}, Pardo and Vittoria Catara and James Abbott and Davide Bulgarelli",

note = "{\textcopyright} 2026 Robertson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.",

year = "2026",

month = jan,

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doi = "10.1128/msphere.00842-25",

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Robertson, S, Mosca, A, Ashraf, S, Corral, A, Alegria Terrazas, R, Arnton, C , Thorpe, P, Morris, JA, Hedley, PE, Babbi, G, Savojardo, C, Martelli, PL, Møller, FD, Nielsen, HN, Leekitcharoenphon, P, Aarestrup, FM, Halder, R, Laczny, CC, Wilmes, P, Pietrantonio, L, Di Cillo, P, Catara, V, Abbott, J & Bulgarelli, D 2026, 'Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants', mSphere. https://doi.org/10.1128/msphere.00842-25

TY - JOUR

T1 - Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants

AU - Robertson, Senga

AU - Mosca, Alexandros

AU - Ashraf, Saira

AU - Corral, Aileen

AU - Alegria Terrazas, Rodrigo

AU - Arnton, Catherine

AU - Thorpe, Peter

AU - Morris, Jenny A.

AU - Hedley, Pete E.

AU - Babbi, Giulia

AU - Savojardo, Castrense

AU - Martelli, Pier Luigi

AU - Møller, Frederik Duus

AU - Nielsen, Hanne Nørgaard

AU - Leekitcharoenphon, Pimlapas

AU - Aarestrup, Frank M.

AU - Halder, Rashi

AU - Laczny, Cedric C.

AU - Wilmes, Paul

AU - Pietrantonio, Laura

AU - Di Cillo, Pardo

AU - Catara, Vittoria

AU - Abbott, James

AU - Bulgarelli, Davide

PY - 2026/1/15

Y1 - 2026/1/15

N2 - Tomato is a staple crop and an excellent model to study host-microbiota interactions in the plant food chain. In this study, we describe a “lab-in-the-field” approach to investigate the microbiota of field-grown tomato plants. High-throughput amplicon sequencing revealed a three-microhabitat partition, phyllosphere, rhizosphere, and root interior, differentiating host-associated communities from the environmental microbiota. An individual bacterium, classified as Acinetobacter sp., emerged as a dominant member of the microbiota at the plant-soil continuum. To gain insights into the functional significance of this enrichment, we subjected rhizosphere specimens to shotgun metagenomics. Similar to the amplicon sequencing survey, a “microhabitat effect,” defined by a set of rhizosphere-enriched functions, was identified. Mobilization of mineral nutrients, as well as adaptation to salinity and polymicrobial communities, including antimicrobial resistance genes (ARGs), emerged as a functional requirement sustaining metagenomic diversification. A metagenome-assembled genome representative of Acinetobacter calcoaceticus was retrieved, and metagenomic reads associated with this species identified a functional specialization for plant-growth promotion traits, such as phosphate solubilization, siderophore production, and reactive oxygen species detoxification, which were similarly represented in a tomato genotype-independent fashion. Our results revealed that the enrichment of a beneficial bacterium capable of alleviating plant abiotic stresses appears decoupled from ARGs facilitating microbiota persistence at the root-soil interface.

AB - Tomato is a staple crop and an excellent model to study host-microbiota interactions in the plant food chain. In this study, we describe a “lab-in-the-field” approach to investigate the microbiota of field-grown tomato plants. High-throughput amplicon sequencing revealed a three-microhabitat partition, phyllosphere, rhizosphere, and root interior, differentiating host-associated communities from the environmental microbiota. An individual bacterium, classified as Acinetobacter sp., emerged as a dominant member of the microbiota at the plant-soil continuum. To gain insights into the functional significance of this enrichment, we subjected rhizosphere specimens to shotgun metagenomics. Similar to the amplicon sequencing survey, a “microhabitat effect,” defined by a set of rhizosphere-enriched functions, was identified. Mobilization of mineral nutrients, as well as adaptation to salinity and polymicrobial communities, including antimicrobial resistance genes (ARGs), emerged as a functional requirement sustaining metagenomic diversification. A metagenome-assembled genome representative of Acinetobacter calcoaceticus was retrieved, and metagenomic reads associated with this species identified a functional specialization for plant-growth promotion traits, such as phosphate solubilization, siderophore production, and reactive oxygen species detoxification, which were similarly represented in a tomato genotype-independent fashion. Our results revealed that the enrichment of a beneficial bacterium capable of alleviating plant abiotic stresses appears decoupled from ARGs facilitating microbiota persistence at the root-soil interface.

KW - food-chain microbiota

KW - tomato

KW - metagenomics

KW - AMR

KW - One Health

U2 - 10.1128/msphere.00842-25

DO - 10.1128/msphere.00842-25

M3 - Article

C2 - 41537582

SN - 2379-5042

JO - mSphere

JF - mSphere

M1 - e00842-25

ER -

Acinetobacter enrichment shapes composition and function of the bacterial microbiota of field-grown tomato plants

Abstract

Keywords

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Controlling mIcRobiomes CircuLations for bEtter food Systems (CIRCLES) (joint with Alma Mater Studiorum - Universita di Bologna as lead, PanepistimioThessalias, Bolton Alimentari and 26 others)

Cite this