Cargando…

Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model

BACKGROUND: The described species from the Metarhizium genus are cosmopolitan fungi that infect arthropod hosts. Interestingly, while some species infect a wide range of hosts (host-generalists), other species infect only a few arthropods (host-specialists). This singular evolutionary trait permits...

Descripción completa

Detalles Bibliográficos
Autores principales: Sbaraini, Nicolau, Guedes, Rafael Lucas Muniz, Andreis, Fábio Carrer, Junges, Ângela, de Morais, Guilherme Loss, Vainstein, Marilene Henning, de Vasconcelos, Ana Tereza Ribeiro, Schrank, Augusto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5088523/
https://www.ncbi.nlm.nih.gov/pubmed/27801295
http://dx.doi.org/10.1186/s12864-016-3067-6
_version_ 1782464111974547456
author Sbaraini, Nicolau
Guedes, Rafael Lucas Muniz
Andreis, Fábio Carrer
Junges, Ângela
de Morais, Guilherme Loss
Vainstein, Marilene Henning
de Vasconcelos, Ana Tereza Ribeiro
Schrank, Augusto
author_facet Sbaraini, Nicolau
Guedes, Rafael Lucas Muniz
Andreis, Fábio Carrer
Junges, Ângela
de Morais, Guilherme Loss
Vainstein, Marilene Henning
de Vasconcelos, Ana Tereza Ribeiro
Schrank, Augusto
author_sort Sbaraini, Nicolau
collection PubMed
description BACKGROUND: The described species from the Metarhizium genus are cosmopolitan fungi that infect arthropod hosts. Interestingly, while some species infect a wide range of hosts (host-generalists), other species infect only a few arthropods (host-specialists). This singular evolutionary trait permits unique comparisons to determine how pathogens and virulence determinants emerge. Among the several virulence determinants that have been described, secondary metabolites (SMs) are suggested to play essential roles during fungal infection. Despite progress in the study of pathogen-host relationships, the majority of genes related to SM production in Metarhizium spp. are uncharacterized, and little is known about their genomic organization, expression and regulation. To better understand how infection conditions may affect SM production in Metarhizium anisopliae, we have performed a deep survey and description of SM biosynthetic gene clusters (BGCs) in M. anisopliae, analyzed RNA-seq data from fungi grown on cattle-tick cuticles, evaluated the differential expression of BGCs, and assessed conservation among the Metarhizium genus. Furthermore, our analysis extended to the construction of a phylogeny for the following three BGCs: a tropolone/citrinin-related compound (MaPKS1), a pseurotin-related compound (MaNRPS-PKS2), and a putative helvolic acid (MaTERP1). RESULTS: Among 73 BGCs identified in M. anisopliae, 20 % were up-regulated during initial tick cuticle infection and presumably possess virulence-related roles. These up-regulated BGCs include known clusters, such as destruxin, NG39x and ferricrocin, together with putative helvolic acid and, pseurotin and tropolone/citrinin-related compound clusters as well as uncharacterized clusters. Furthermore, several previously characterized and putative BGCs were silent or down-regulated in initial infection conditions, indicating minor participation over the course of infection. Interestingly, several up-regulated BGCs were not conserved in host-specialist species from the Metarhizium genus, indicating differences in the metabolic strategies employed by generalist and specialist species to overcome and kill their host. These differences in metabolic potential may have been partially shaped by horizontal gene transfer (HGT) events, as our phylogenetic analysis provided evidence that the putative helvolic acid cluster in Metarhizium spp. originated from an HGT event. CONCLUSIONS: Several unknown BGCs are described, and aspects of their organization, regulation and origin are discussed, providing further support for the impact of SM on the Metarhizium genus lifestyle and infection process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3067-6) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5088523
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-50885232016-11-07 Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model Sbaraini, Nicolau Guedes, Rafael Lucas Muniz Andreis, Fábio Carrer Junges, Ângela de Morais, Guilherme Loss Vainstein, Marilene Henning de Vasconcelos, Ana Tereza Ribeiro Schrank, Augusto BMC Genomics Research BACKGROUND: The described species from the Metarhizium genus are cosmopolitan fungi that infect arthropod hosts. Interestingly, while some species infect a wide range of hosts (host-generalists), other species infect only a few arthropods (host-specialists). This singular evolutionary trait permits unique comparisons to determine how pathogens and virulence determinants emerge. Among the several virulence determinants that have been described, secondary metabolites (SMs) are suggested to play essential roles during fungal infection. Despite progress in the study of pathogen-host relationships, the majority of genes related to SM production in Metarhizium spp. are uncharacterized, and little is known about their genomic organization, expression and regulation. To better understand how infection conditions may affect SM production in Metarhizium anisopliae, we have performed a deep survey and description of SM biosynthetic gene clusters (BGCs) in M. anisopliae, analyzed RNA-seq data from fungi grown on cattle-tick cuticles, evaluated the differential expression of BGCs, and assessed conservation among the Metarhizium genus. Furthermore, our analysis extended to the construction of a phylogeny for the following three BGCs: a tropolone/citrinin-related compound (MaPKS1), a pseurotin-related compound (MaNRPS-PKS2), and a putative helvolic acid (MaTERP1). RESULTS: Among 73 BGCs identified in M. anisopliae, 20 % were up-regulated during initial tick cuticle infection and presumably possess virulence-related roles. These up-regulated BGCs include known clusters, such as destruxin, NG39x and ferricrocin, together with putative helvolic acid and, pseurotin and tropolone/citrinin-related compound clusters as well as uncharacterized clusters. Furthermore, several previously characterized and putative BGCs were silent or down-regulated in initial infection conditions, indicating minor participation over the course of infection. Interestingly, several up-regulated BGCs were not conserved in host-specialist species from the Metarhizium genus, indicating differences in the metabolic strategies employed by generalist and specialist species to overcome and kill their host. These differences in metabolic potential may have been partially shaped by horizontal gene transfer (HGT) events, as our phylogenetic analysis provided evidence that the putative helvolic acid cluster in Metarhizium spp. originated from an HGT event. CONCLUSIONS: Several unknown BGCs are described, and aspects of their organization, regulation and origin are discussed, providing further support for the impact of SM on the Metarhizium genus lifestyle and infection process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3067-6) contains supplementary material, which is available to authorized users. BioMed Central 2016-10-25 /pmc/articles/PMC5088523/ /pubmed/27801295 http://dx.doi.org/10.1186/s12864-016-3067-6 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Sbaraini, Nicolau
Guedes, Rafael Lucas Muniz
Andreis, Fábio Carrer
Junges, Ângela
de Morais, Guilherme Loss
Vainstein, Marilene Henning
de Vasconcelos, Ana Tereza Ribeiro
Schrank, Augusto
Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title_full Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title_fullStr Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title_full_unstemmed Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title_short Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
title_sort secondary metabolite gene clusters in the entomopathogen fungus metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5088523/
https://www.ncbi.nlm.nih.gov/pubmed/27801295
http://dx.doi.org/10.1186/s12864-016-3067-6
work_keys_str_mv AT sbaraininicolau secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT guedesrafaellucasmuniz secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT andreisfabiocarrer secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT jungesangela secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT demoraisguilhermeloss secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT vainsteinmarilenehenning secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT devasconcelosanaterezaribeiro secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel
AT schrankaugusto secondarymetabolitegeneclustersintheentomopathogenfungusmetarhiziumanisopliaegenomeidentificationandpatternsofexpressioninacuticleinfectionmodel