Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum

Abstract The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecu...

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Main Authors: Maria Isabella Prigigallo, Alessia Staropoli, Francesco Vinale, Giovanni Bubici
Format: Article
Language:English
Published: Wiley 2023-12-01
Series:Microbial Biotechnology
Online Access:https://doi.org/10.1111/1751-7915.14311
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author Maria Isabella Prigigallo
Alessia Staropoli
Francesco Vinale
Giovanni Bubici
author_facet Maria Isabella Prigigallo
Alessia Staropoli
Francesco Vinale
Giovanni Bubici
author_sort Maria Isabella Prigigallo
collection DOAJ
description Abstract The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecular level of two elite biological control agents (BCAs), that is Streptomyces microflavus strain AtB‐42 and Trichoderma harzianum strain M10, to understand their attitude to cooperate in a consortium. In vitro, we observed a strong cross‐antagonism between AtB‐42 and M10 in agar plates due to diffusible metabolites and volatile organic compounds. In liquid co‐cultures, M10 hindered the growth of AtB‐42 very likely because of secondary metabolites and strong competition for the nutrients. The interaction in the co‐culture induced extensive transcriptional reprogramming in both strains, especially in the pathways related to ribosomes, protein synthesis, and oxidoreductase activity, suggesting that each strain recognized the counterpart and activated its defence responses. The metabolome of both strains was also significantly affected. In contrast, in the soil, M10 growth was partially contrasted by AtB‐42. The roots of tomato seedlings inoculated with the consortium appeared smaller than the control and single‐strain‐inoculated plants, indicating that plants diverted some energy from the development to defence activation, as evidenced by the leaf transcriptome. The consortium induced a stronger transcriptional change compared to the single inoculants, as demonstrated by a higher number of differentially expressed genes. Although the cross‐antagonism observed in vitro, the two strains exerted a synergistic effect on tomato seedlings by inducing resistance responses stronger than the single inoculants. Our observations pose a question on the usefulness of the sole in vitro assays for selecting BCAs to construct a consortium. In vivo experiments should be preferred, and transcriptomics may greatly help to elucidate the activity of the BCAs beyond the phenotypic effects on the plant.
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spelling doaj.art-3c6dc897f5074fb0b8093e771a070a032023-11-29T14:27:04ZengWileyMicrobial Biotechnology1751-79152023-12-0116122292231210.1111/1751-7915.14311Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianumMaria Isabella Prigigallo0Alessia Staropoli1Francesco Vinale2Giovanni Bubici3Istituto per la Protezione Sostenibile delle Piante Consiglio Nazionale delle Ricerche Bari ItalyIstituto per la Protezione Sostenibile delle Piante Consiglio Nazionale delle Ricerche Portici ItalyDipartimento di Medicina Veterinaria e Produzioni Animali Università degli Studi di Napoli Federico II Naples ItalyIstituto per la Protezione Sostenibile delle Piante Consiglio Nazionale delle Ricerche Bari ItalyAbstract The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecular level of two elite biological control agents (BCAs), that is Streptomyces microflavus strain AtB‐42 and Trichoderma harzianum strain M10, to understand their attitude to cooperate in a consortium. In vitro, we observed a strong cross‐antagonism between AtB‐42 and M10 in agar plates due to diffusible metabolites and volatile organic compounds. In liquid co‐cultures, M10 hindered the growth of AtB‐42 very likely because of secondary metabolites and strong competition for the nutrients. The interaction in the co‐culture induced extensive transcriptional reprogramming in both strains, especially in the pathways related to ribosomes, protein synthesis, and oxidoreductase activity, suggesting that each strain recognized the counterpart and activated its defence responses. The metabolome of both strains was also significantly affected. In contrast, in the soil, M10 growth was partially contrasted by AtB‐42. The roots of tomato seedlings inoculated with the consortium appeared smaller than the control and single‐strain‐inoculated plants, indicating that plants diverted some energy from the development to defence activation, as evidenced by the leaf transcriptome. The consortium induced a stronger transcriptional change compared to the single inoculants, as demonstrated by a higher number of differentially expressed genes. Although the cross‐antagonism observed in vitro, the two strains exerted a synergistic effect on tomato seedlings by inducing resistance responses stronger than the single inoculants. Our observations pose a question on the usefulness of the sole in vitro assays for selecting BCAs to construct a consortium. In vivo experiments should be preferred, and transcriptomics may greatly help to elucidate the activity of the BCAs beyond the phenotypic effects on the plant.https://doi.org/10.1111/1751-7915.14311
spellingShingle Maria Isabella Prigigallo
Alessia Staropoli
Francesco Vinale
Giovanni Bubici
Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
Microbial Biotechnology
title Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_full Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_fullStr Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_full_unstemmed Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_short Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_sort interactions between plant beneficial microorganisms in a consortium streptomyces microflavus and trichoderma harzianum
url https://doi.org/10.1111/1751-7915.14311
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AT francescovinale interactionsbetweenplantbeneficialmicroorganismsinaconsortiumstreptomycesmicroflavusandtrichodermaharzianum
AT giovannibubici interactionsbetweenplantbeneficialmicroorganismsinaconsortiumstreptomycesmicroflavusandtrichodermaharzianum