Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis

In the myrmecophytic mutualistic relationship between Azteca ants and Cecropia plants both species receive protection and exchange nutrients. The presence of microorganisms in this symbiotic system has been reported, and the symbiotic role of some fungi involved in the myrmecophytic interactions has...

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Main Authors: Taise T. H. Fukuda, Camila F. Pereira, Weilan G. P. Melo, Carla Menegatti, Paulo H. M. Andrade, Milton Groppo, Paulo T. Lacava, Cameron R. Currie, Mônica T. Pupo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.621274/full
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spelling doaj-6787c4a24efc42ad90bf3da76f77508d2021-02-01T04:52:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-02-011210.3389/fmicb.2021.621274621274Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant SymbiosisTaise T. H. Fukuda0Camila F. Pereira1Weilan G. P. Melo2Carla Menegatti3Paulo H. M. Andrade4Milton Groppo5Paulo T. Lacava6Cameron R. Currie7Mônica T. Pupo8School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilSchool of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilSchool of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilSchool of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilLaboratory of Microbiology and Biomolecules, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, BrazilLaboratory of Plant Systematics, Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilLaboratory of Microbiology and Biomolecules, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, BrazilDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesSchool of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, BrazilIn the myrmecophytic mutualistic relationship between Azteca ants and Cecropia plants both species receive protection and exchange nutrients. The presence of microorganisms in this symbiotic system has been reported, and the symbiotic role of some fungi involved in the myrmecophytic interactions has been described. In this work we focus on bacteria within this mutualism, conducting isolations and screening for antimicrobial activities, genome sequencing, and biochemical characterization. We show that Pantoea, Rhizobium, Methylobacterium, Streptomyces and Pseudomonas are the most common cultivable genera of bacteria. Interestingly, Pseudomonas spp. isolates showed potent activity against 83% of the pathogens tested in our antimicrobial activity assays, including a phytopathogenic fungus isolated from Cecropia samples. Given the predicted nitrogen limitations associated with the fungal patches within this myrmecophyte, we performed nitrogen fixation analyses on the bacterial isolates within the Proteobacteria and show the potential for nitrogen fixation in Pseudomonas strains. The genome of one Pseudomonas strain was sequenced and analyzed. The gene cluster involved in the biosynthesis of cyclic lipodepsipeptides (CLPs) was identified, and we found mutations that may be related to the loss of function in the dual epimerization/condensation domains. The compound was isolated, and its structure was determined, corresponding to the antifungal viscosinamide. Our findings of diazotrophy and production of viscosinamide in multiple Pseudomonas isolates suggests that this bacterial genus may play an important role in the Cecropia-Azteca symbiosis.https://www.frontiersin.org/articles/10.3389/fmicb.2021.621274/fullmyrmecophytesbacteriaantimicrobial activitiesnitrogen fixationgenome miningPseudomonas
collection DOAJ
language English
format Article
sources DOAJ
author Taise T. H. Fukuda
Camila F. Pereira
Weilan G. P. Melo
Carla Menegatti
Paulo H. M. Andrade
Milton Groppo
Paulo T. Lacava
Cameron R. Currie
Mônica T. Pupo
spellingShingle Taise T. H. Fukuda
Camila F. Pereira
Weilan G. P. Melo
Carla Menegatti
Paulo H. M. Andrade
Milton Groppo
Paulo T. Lacava
Cameron R. Currie
Mônica T. Pupo
Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
Frontiers in Microbiology
myrmecophytes
bacteria
antimicrobial activities
nitrogen fixation
genome mining
Pseudomonas
author_facet Taise T. H. Fukuda
Camila F. Pereira
Weilan G. P. Melo
Carla Menegatti
Paulo H. M. Andrade
Milton Groppo
Paulo T. Lacava
Cameron R. Currie
Mônica T. Pupo
author_sort Taise T. H. Fukuda
title Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
title_short Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
title_full Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
title_fullStr Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
title_full_unstemmed Insights Into the Ecological Role of Pseudomonas spp. in an Ant-plant Symbiosis
title_sort insights into the ecological role of pseudomonas spp. in an ant-plant symbiosis
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-02-01
description In the myrmecophytic mutualistic relationship between Azteca ants and Cecropia plants both species receive protection and exchange nutrients. The presence of microorganisms in this symbiotic system has been reported, and the symbiotic role of some fungi involved in the myrmecophytic interactions has been described. In this work we focus on bacteria within this mutualism, conducting isolations and screening for antimicrobial activities, genome sequencing, and biochemical characterization. We show that Pantoea, Rhizobium, Methylobacterium, Streptomyces and Pseudomonas are the most common cultivable genera of bacteria. Interestingly, Pseudomonas spp. isolates showed potent activity against 83% of the pathogens tested in our antimicrobial activity assays, including a phytopathogenic fungus isolated from Cecropia samples. Given the predicted nitrogen limitations associated with the fungal patches within this myrmecophyte, we performed nitrogen fixation analyses on the bacterial isolates within the Proteobacteria and show the potential for nitrogen fixation in Pseudomonas strains. The genome of one Pseudomonas strain was sequenced and analyzed. The gene cluster involved in the biosynthesis of cyclic lipodepsipeptides (CLPs) was identified, and we found mutations that may be related to the loss of function in the dual epimerization/condensation domains. The compound was isolated, and its structure was determined, corresponding to the antifungal viscosinamide. Our findings of diazotrophy and production of viscosinamide in multiple Pseudomonas isolates suggests that this bacterial genus may play an important role in the Cecropia-Azteca symbiosis.
topic myrmecophytes
bacteria
antimicrobial activities
nitrogen fixation
genome mining
Pseudomonas
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.621274/full
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