Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants

Abstract The fungus-growing ant-microbe symbiosis is an ideal system to study chemistry-based microbial interactions due to the wealth of microbial interactions described, and the lack of information on the molecules involved therein. In this study, we employed a combination of MALDI imaging mass sp...

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Main Authors: Cristopher A. Boya P., Hermógenes Fernández-Marín, Luis C. Mejía, Carmenza Spadafora, Pieter C. Dorrestein, Marcelino Gutiérrez
Format: Article
Language:English
Published: Nature Publishing Group 2017-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-05515-6
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spelling doaj-083d69c2ffe840dc9419c320c5222dfa2020-12-08T02:06:48ZengNature Publishing GroupScientific Reports2045-23222017-07-017111310.1038/s41598-017-05515-6Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing antsCristopher A. Boya P.0Hermógenes Fernández-Marín1Luis C. Mejía2Carmenza Spadafora3Pieter C. Dorrestein4Marcelino Gutiérrez5Centro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP)Centro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP)Centro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP)Centro de Biología Celular y Molecular de Enfermedades, INDICASAT AIPCollaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California at San DiegoCentro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP)Abstract The fungus-growing ant-microbe symbiosis is an ideal system to study chemistry-based microbial interactions due to the wealth of microbial interactions described, and the lack of information on the molecules involved therein. In this study, we employed a combination of MALDI imaging mass spectrometry (MALDI-IMS) and MS/MS molecular networking to study chemistry-based microbial interactions in this system. MALDI IMS was used to visualize the distribution of antimicrobials at the inhibition zone between bacteria associated to the ant Acromyrmex echinatior and the fungal pathogen Escovopsis sp. MS/MS molecular networking was used for the dereplication of compounds found at the inhibition zones. We identified the antibiotics actinomycins D, X2 and X0β, produced by the bacterium Streptomyces CBR38; and the macrolides elaiophylin, efomycin A and efomycin G, produced by the bacterium Streptomyces CBR53.These metabolites were found at the inhibition zones using MALDI IMS and were identified using MS/MS molecular networking. Additionally, three shearinines D, F, and J produced by the fungal pathogen Escovopsis TZ49 were detected. This is the first report of elaiophylins, actinomycin X0β and shearinines in the fungus-growing ant symbiotic system. These results suggest a secondary prophylactic use of these antibiotics by A. echinatior because of their permanent production by the bacteria.https://doi.org/10.1038/s41598-017-05515-6
collection DOAJ
language English
format Article
sources DOAJ
author Cristopher A. Boya P.
Hermógenes Fernández-Marín
Luis C. Mejía
Carmenza Spadafora
Pieter C. Dorrestein
Marcelino Gutiérrez
spellingShingle Cristopher A. Boya P.
Hermógenes Fernández-Marín
Luis C. Mejía
Carmenza Spadafora
Pieter C. Dorrestein
Marcelino Gutiérrez
Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
Scientific Reports
author_facet Cristopher A. Boya P.
Hermógenes Fernández-Marín
Luis C. Mejía
Carmenza Spadafora
Pieter C. Dorrestein
Marcelino Gutiérrez
author_sort Cristopher A. Boya P.
title Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
title_short Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
title_full Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
title_fullStr Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
title_full_unstemmed Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
title_sort imaging mass spectrometry and ms/ms molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-07-01
description Abstract The fungus-growing ant-microbe symbiosis is an ideal system to study chemistry-based microbial interactions due to the wealth of microbial interactions described, and the lack of information on the molecules involved therein. In this study, we employed a combination of MALDI imaging mass spectrometry (MALDI-IMS) and MS/MS molecular networking to study chemistry-based microbial interactions in this system. MALDI IMS was used to visualize the distribution of antimicrobials at the inhibition zone between bacteria associated to the ant Acromyrmex echinatior and the fungal pathogen Escovopsis sp. MS/MS molecular networking was used for the dereplication of compounds found at the inhibition zones. We identified the antibiotics actinomycins D, X2 and X0β, produced by the bacterium Streptomyces CBR38; and the macrolides elaiophylin, efomycin A and efomycin G, produced by the bacterium Streptomyces CBR53.These metabolites were found at the inhibition zones using MALDI IMS and were identified using MS/MS molecular networking. Additionally, three shearinines D, F, and J produced by the fungal pathogen Escovopsis TZ49 were detected. This is the first report of elaiophylins, actinomycin X0β and shearinines in the fungus-growing ant symbiotic system. These results suggest a secondary prophylactic use of these antibiotics by A. echinatior because of their permanent production by the bacteria.
url https://doi.org/10.1038/s41598-017-05515-6
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