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Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria

BACKGROUND: In recent years, the number of human infections caused by opportunistic pathogens has increased dramatically. Plant rhizospheres are one of the most typical natural reservoirs for these pathogens but they also represent a great source for beneficial microbes with potential for biotechnol...

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Autores principales: Alavi, Peyman, Starcher, Margaret R, Thallinger, Gerhard G, Zachow, Christin, Müller, Henry, Berg, Gabriele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4101175/
https://www.ncbi.nlm.nih.gov/pubmed/24939220
http://dx.doi.org/10.1186/1471-2164-15-482
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author Alavi, Peyman
Starcher, Margaret R
Thallinger, Gerhard G
Zachow, Christin
Müller, Henry
Berg, Gabriele
author_facet Alavi, Peyman
Starcher, Margaret R
Thallinger, Gerhard G
Zachow, Christin
Müller, Henry
Berg, Gabriele
author_sort Alavi, Peyman
collection PubMed
description BACKGROUND: In recent years, the number of human infections caused by opportunistic pathogens has increased dramatically. Plant rhizospheres are one of the most typical natural reservoirs for these pathogens but they also represent a great source for beneficial microbes with potential for biotechnological applications. However, understanding the natural variation and possible differences between pathogens and beneficials is the main challenge in furthering these possibilities. The genus Stenotrophomonas contains representatives found to be associated with human and plant host. RESULTS: We used comparative genomics as well as transcriptomic and physiological approaches to detect significant borders between the Stenotrophomonas strains: the multi-drug resistant pathogenic S. maltophilia and the plant-associated strains S. maltophilia R551-3 and S. rhizophila DSM14405(T) (both are biocontrol agents). We found an overall high degree of sequence similarity between the genomes of all three strains. Despite the notable similarity in potential factors responsible for host invasion and antibiotic resistance, other factors including several crucial virulence factors and heat shock proteins were absent in the plant-associated DSM14405(T). Instead, S. rhizophila DSM14405(T) possessed unique genes for the synthesis and transport of the plant-protective spermidine, plant cell-wall degrading enzymes, and high salinity tolerance. Moreover, the presence or absence of bacterial growth at 37°C was identified as a very simple method in differentiating between pathogenic and non-pathogenic isolates. DSM14405(T) is not able to grow at this human-relevant temperature, most likely in great part due to the absence of heat shock genes and perhaps also because of the up-regulation at increased temperatures of several genes involved in a suicide mechanism. CONCLUSIONS: While this study is important for understanding the mechanisms behind the emerging pattern of infectious diseases, it is, to our knowledge, the first of its kind to assess the risk of beneficial strains for biotechnological applications. We identified certain traits typical of pathogens such as growth at the human body temperature together with the production of heat shock proteins as opposed to a temperature-regulated suicide system that is harnessed by beneficials. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-482) contains supplementary material, which is available to authorized users.
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spelling pubmed-41011752014-07-18 Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria Alavi, Peyman Starcher, Margaret R Thallinger, Gerhard G Zachow, Christin Müller, Henry Berg, Gabriele BMC Genomics Research Article BACKGROUND: In recent years, the number of human infections caused by opportunistic pathogens has increased dramatically. Plant rhizospheres are one of the most typical natural reservoirs for these pathogens but they also represent a great source for beneficial microbes with potential for biotechnological applications. However, understanding the natural variation and possible differences between pathogens and beneficials is the main challenge in furthering these possibilities. The genus Stenotrophomonas contains representatives found to be associated with human and plant host. RESULTS: We used comparative genomics as well as transcriptomic and physiological approaches to detect significant borders between the Stenotrophomonas strains: the multi-drug resistant pathogenic S. maltophilia and the plant-associated strains S. maltophilia R551-3 and S. rhizophila DSM14405(T) (both are biocontrol agents). We found an overall high degree of sequence similarity between the genomes of all three strains. Despite the notable similarity in potential factors responsible for host invasion and antibiotic resistance, other factors including several crucial virulence factors and heat shock proteins were absent in the plant-associated DSM14405(T). Instead, S. rhizophila DSM14405(T) possessed unique genes for the synthesis and transport of the plant-protective spermidine, plant cell-wall degrading enzymes, and high salinity tolerance. Moreover, the presence or absence of bacterial growth at 37°C was identified as a very simple method in differentiating between pathogenic and non-pathogenic isolates. DSM14405(T) is not able to grow at this human-relevant temperature, most likely in great part due to the absence of heat shock genes and perhaps also because of the up-regulation at increased temperatures of several genes involved in a suicide mechanism. CONCLUSIONS: While this study is important for understanding the mechanisms behind the emerging pattern of infectious diseases, it is, to our knowledge, the first of its kind to assess the risk of beneficial strains for biotechnological applications. We identified certain traits typical of pathogens such as growth at the human body temperature together with the production of heat shock proteins as opposed to a temperature-regulated suicide system that is harnessed by beneficials. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-482) contains supplementary material, which is available to authorized users. BioMed Central 2014-06-18 /pmc/articles/PMC4101175/ /pubmed/24939220 http://dx.doi.org/10.1186/1471-2164-15-482 Text en © Alavi et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Alavi, Peyman
Starcher, Margaret R
Thallinger, Gerhard G
Zachow, Christin
Müller, Henry
Berg, Gabriele
Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title_full Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title_fullStr Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title_full_unstemmed Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title_short Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
title_sort stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4101175/
https://www.ncbi.nlm.nih.gov/pubmed/24939220
http://dx.doi.org/10.1186/1471-2164-15-482
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