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Impact of quorum sensing from native peanut phosphate solubilizing Serratia sp. S119 strain on interactions with agronomically important crops

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Abstract

Bacteria communicate with each other using a language based on the use of autoinducer molecules (AI) to collectively control gene expression through the process known as quorum sensing (QS). The N-acylhomoserine lactones (AHLs) are the most common AIs known in Gram-negative bacteria. Numerous genes encoding QS systems have been reported in plant beneficial endophytic bacterial genomes although there are fewer studies evaluating the participation of QS in the mechanisms of plant growth promotion. The aim of this study was to describe the genetic background and the types of AHLs produced by a phosphate-solubilizing bacterial strain isolated from the roots of peanut Serratia sp. S119, and to evaluate the participation of these AIs in promoting the growth of plants of agronomic importance.

Bioinformatics analysis indicated that the genome of S119 strain harbors genes encoding proteins involved in the production and detection of AHLs. This strain was found to produce the QS molecules C8-HSL, C10-HSL, 3-OH-C8-HSL and 3-OH-C10-HSL with the latter being the most abundant AHL. By overexpressing a heterologous lactonase enzyme in Serratia sp. S119, this strain was depleted in the production of all AHLs with the exception of 3-OH-C10-HSL which levels were reduced by 50%. The ability to solubilize phosphate, produce biofilms and promote plant growth was analyzed in the AHL attenuated strain. This strain was able to maintain the ability to solubilize phosphate while biofilm production was significantly reduced. Plant inoculation assays with the QS attenuated strain showed differences responses on growth parameters of the three plants employed.

These results indicate that the AHLs from the phosphate solubilizing Serratia sp. S119 strain may not affect its ability to solubilize phosphate. However, they play a role in biofilm formation that is a key trait for bacterial colonization in its interaction with plant species.

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Acknowledgements

The authors would like to thank for the help provided by Dr. Stephan Heeb and Dr. Manuel Romero (Centre for Biomolecular Sciences, University of Nottingham) for sending the strains E.coli pME6863 and pME6000, and in the protocol to study the production of biofilms. The authors thanks to Dr. Fernando Ibañez (Instituto de Investigaciones Agrobiotecnológicas UNRC-CONICET) for the assistance provided in the phylogenetic analysis of the amino acid sequence of LuxI proteins.

This research was supported by Facultad de Ciencias Exactas y Naturales de la Universidad Nacional de La Pampa (FCEyN-UNLPam), Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto (SECYT-UNRC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and the National Biofilms Innovation Centre (NBIC) which is an Innovation and Knowledge Centre funded by the Biotechnology and Biological Sciences Research 1549 Council, Innovate UK and Hartree Centre [Award Number 1550 BB/R012415/1].

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Authors and Affiliations

  1. Departamento de Química, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa, Provincia de La Pampa, Ruta Nacional 35 km 330, 6300, Santa Rosa, CP, Argentina

    Cinthia Tamara Lucero, Graciela Susana Lorda & Mariela Lis Ambrosino

  2. National Biofilms Innovation Centre, Biodiscovery Institute, School of Life Sciences, University of Nottingham, NG7 2RD, Nottingham, UK

    Nigel Halliday & Miguel Cámara

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), 6300, Santa Rosa, Provincia de La Pampa, Argentina

    Mariela Lis Ambrosino

  4. Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Instituto de Investigaciones Agrobiotecnológicas (INIAB), Universidad Nacional de Río Cuarto, Agencia Postal 3, 5800, Río Cuarto, Córdoba, Argentina

    Tania Taurian

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Lucero, C.T., Lorda, G.S., Halliday, N. et al. Impact of quorum sensing from native peanut phosphate solubilizing Serratia sp. S119 strain on interactions with agronomically important crops. Symbiosis 89, 107–121 (2023). https://doi.org/10.1007/s13199-022-00893-6

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