Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis

Annette A. Angus, Christina M. Agapakis, Stephanie Fong, Shailaja Yerrapragada, Paulina Estrada-de Los Santos, Paul Yang, Nannie Song, Stephanie Kano, Jésus Caballero-Mellado, Sergio M. De Faria, Felix D. Dakora, George Weinstock, Ann M. Hirsch

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low. © 2014 Angus et al.
Original languageAmerican English
JournalPLoS ONE
DOIs
StatePublished - 8 Jan 2014

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Burkholderia
pathogenesis
plant growth
Pathogens
Growth
Malleus
infection
Mammals
pathogens
Climate Change
Immune system
Opportunistic Infections
Caenorhabditis elegans
Fertilizers
Xenobiotics
xenobiotics
Bioinformatics
Infection
Computational Biology
Agriculture

Cite this

Angus, Annette A. ; Agapakis, Christina M. ; Fong, Stephanie ; Yerrapragada, Shailaja ; Estrada-de Los Santos, Paulina ; Yang, Paul ; Song, Nannie ; Kano, Stephanie ; Caballero-Mellado, Jésus ; De Faria, Sergio M. ; Dakora, Felix D. ; Weinstock, George ; Hirsch, Ann M. / Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. In: PLoS ONE. 2014.
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abstract = "Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low. {\circledC} 2014 Angus et al.",
author = "Angus, {Annette A.} and Agapakis, {Christina M.} and Stephanie Fong and Shailaja Yerrapragada and {Estrada-de Los Santos}, Paulina and Paul Yang and Nannie Song and Stephanie Kano and J{\'e}sus Caballero-Mellado and {De Faria}, {Sergio M.} and Dakora, {Felix D.} and George Weinstock and Hirsch, {Ann M.}",
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Angus, AA, Agapakis, CM, Fong, S, Yerrapragada, S, Estrada-de Los Santos, P, Yang, P, Song, N, Kano, S, Caballero-Mellado, J, De Faria, SM, Dakora, FD, Weinstock, G & Hirsch, AM 2014, 'Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis', PLoS ONE. https://doi.org/10.1371/journal.pone.0083779

Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. / Angus, Annette A.; Agapakis, Christina M.; Fong, Stephanie; Yerrapragada, Shailaja; Estrada-de Los Santos, Paulina; Yang, Paul; Song, Nannie; Kano, Stephanie; Caballero-Mellado, Jésus; De Faria, Sergio M.; Dakora, Felix D.; Weinstock, George; Hirsch, Ann M.

In: PLoS ONE, 08.01.2014.

Research output: Contribution to journalArticle

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AU - Angus, Annette A.

AU - Agapakis, Christina M.

AU - Fong, Stephanie

AU - Yerrapragada, Shailaja

AU - Estrada-de Los Santos, Paulina

AU - Yang, Paul

AU - Song, Nannie

AU - Kano, Stephanie

AU - Caballero-Mellado, Jésus

AU - De Faria, Sergio M.

AU - Dakora, Felix D.

AU - Weinstock, George

AU - Hirsch, Ann M.

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AB - Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low. © 2014 Angus et al.

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