Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins

Charley Christian Staats; Angela Junges; Rafael Lucas Muniz Guedes; Claudia Elizabeth Thompson; Guilherme Loss de Morais; Juliano Tomazzoni Boldo; Luiz Gonzaga Paula de Almeida; Fábio Carrer Andreis; Alexandra Lehmkuhl Gerber; Nicolau Sbaraini; Rana Louise de Andrade da Paixão; Leonardo Broetto; Melissa Landell; Lucélia Santi; Walter Orlando Beys-da-Silva; Carolina Pereira Silveira; Thaiane Rispoli Serrano; Eder Silva de Oliveira; Lívia Kmetzsch; Marilene Henning Vainstein; Ana Tereza Ribeiro de Vasconcelos; Augusto Schrank

doi:10.1186/1471-2164-15-822

Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins

Charley Christian Staats, Angela Junges, Rafael Lucas Muniz Guedes, Claudia Elizabeth Thompson, Guilherme Loss de Morais, Juliano Tomazzoni Boldo, Luiz Gonzaga Paula de Almeida, Fábio Carrer Andreis, Alexandra Lehmkuhl Gerber, Nicolau Sbaraini, Rana Louise de Andrade da Paixão, Leonardo Broetto, Melissa Landell, Lucélia Santi, Walter Orlando Beys-da-Silva, Carolina Pereira Silveira, Thaiane Rispoli Serrano, Eder Silva de Oliveira, Lívia Kmetzsch, Marilene Henning VainsteinAna Tereza Ribeiro de Vasconcelos, Augusto Schrank

Research output: Contribution to journal › Article › peer-review

46 Citations (Scopus)

Abstract

BACKGROUND: Metarhizium anisopliae is an entomopathogenic fungus used in the biological control of some agricultural insect pests, and efforts are underway to use this fungus in the control of insect-borne human diseases. A large repertoire of proteins must be secreted by M. anisopliae to cope with the various available nutrients as this fungus switches through different lifestyles, i.e., from a saprophytic, to an infectious, to a plant endophytic stage. To further evaluate the predicted secretome of M. anisopliae, we employed genomic and transcriptomic analyses, coupled with phylogenomic analysis, focusing on the identification and characterization of secreted proteins.

RESULTS: We determined the M. anisopliae E6 genome sequence and compared this sequence to other entomopathogenic fungi genomes. A robust pipeline was generated to evaluate the predicted secretomes of M. anisopliae and 15 other filamentous fungi, leading to the identification of a core of secreted proteins. Transcriptomic analysis using the tick Rhipicephalus microplus cuticle as an infection model during two periods of infection (48 and 144 h) allowed the identification of several differentially expressed genes. This analysis concluded that a large proportion of the predicted secretome coding genes contained altered transcript levels in the conditions analyzed in this study. In addition, some specific secreted proteins from Metarhizium have an evolutionary history similar to orthologs found in Beauveria/Cordyceps. This similarity suggests that a set of secreted proteins has evolved to participate in entomopathogenicity.

CONCLUSIONS: The data presented represents an important step to the characterization of the role of secreted proteins in the virulence and pathogenicity of M. anisopliae.

Original language	English
Pages (from-to)	822
Journal	BMC Genomics
Volume	15
DOIs	https://doi.org/10.1186/1471-2164-15-822
Publication status	Published - 29 Sept 2014
Externally published	Yes

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10.1186/1471-2164-15-822

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Staats, C. C., Junges, A., Guedes, R. L. M., Thompson, C. E., de Morais, G. L., Boldo, J. T., de Almeida, L. G. P., Andreis, F. C., Gerber, A. L., Sbaraini, N., da Paixão, R. L. D. A., Broetto, L., Landell, M., Santi, L., Beys-da-Silva, W. O., Silveira, C. P., Serrano, T. R., de Oliveira, E. S., Kmetzsch, L., ... Schrank, A. (2014). Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics, 15, 822. https://doi.org/10.1186/1471-2164-15-822

@article{1af94470254940288ffdd64b4091b5eb,

title = "Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins",

abstract = "BACKGROUND: Metarhizium anisopliae is an entomopathogenic fungus used in the biological control of some agricultural insect pests, and efforts are underway to use this fungus in the control of insect-borne human diseases. A large repertoire of proteins must be secreted by M. anisopliae to cope with the various available nutrients as this fungus switches through different lifestyles, i.e., from a saprophytic, to an infectious, to a plant endophytic stage. To further evaluate the predicted secretome of M. anisopliae, we employed genomic and transcriptomic analyses, coupled with phylogenomic analysis, focusing on the identification and characterization of secreted proteins.RESULTS: We determined the M. anisopliae E6 genome sequence and compared this sequence to other entomopathogenic fungi genomes. A robust pipeline was generated to evaluate the predicted secretomes of M. anisopliae and 15 other filamentous fungi, leading to the identification of a core of secreted proteins. Transcriptomic analysis using the tick Rhipicephalus microplus cuticle as an infection model during two periods of infection (48 and 144 h) allowed the identification of several differentially expressed genes. This analysis concluded that a large proportion of the predicted secretome coding genes contained altered transcript levels in the conditions analyzed in this study. In addition, some specific secreted proteins from Metarhizium have an evolutionary history similar to orthologs found in Beauveria/Cordyceps. This similarity suggests that a set of secreted proteins has evolved to participate in entomopathogenicity.CONCLUSIONS: The data presented represents an important step to the characterization of the role of secreted proteins in the virulence and pathogenicity of M. anisopliae.",

keywords = "Animals, Comparative Genomic Hybridization, Fungal Proteins/genetics, Gene Expression Profiling, Genome, Fungal, Host-Pathogen Interactions/genetics, Metarhizium/classification, Phylogeny, Rhipicephalus/metabolism, Sequence Analysis, RNA",

author = "Staats, {Charley Christian} and Angela Junges and Guedes, {Rafael Lucas Muniz} and Thompson, {Claudia Elizabeth} and {de Morais}, {Guilherme Loss} and Boldo, {Juliano Tomazzoni} and {de Almeida}, {Luiz Gonzaga Paula} and Andreis, {F{\'a}bio Carrer} and Gerber, {Alexandra Lehmkuhl} and Nicolau Sbaraini and {da Paix{\~a}o}, {Rana Louise de Andrade} and Leonardo Broetto and Melissa Landell and Luc{\'e}lia Santi and Beys-da-Silva, {Walter Orlando} and Silveira, {Carolina Pereira} and Serrano, {Thaiane Rispoli} and {de Oliveira}, {Eder Silva} and L{\'i}via Kmetzsch and Vainstein, {Marilene Henning} and {de Vasconcelos}, {Ana Tereza Ribeiro} and Augusto Schrank",

year = "2014",

month = sep,

day = "29",

doi = "10.1186/1471-2164-15-822",

language = "English",

volume = "15",

pages = "822",

journal = "BMC Genomics",

issn = "1471-2164",

publisher = "BioMed Central",

}

Staats, CC, Junges, A, Guedes, RLM, Thompson, CE, de Morais, GL, Boldo, JT, de Almeida, LGP, Andreis, FC, Gerber, AL, Sbaraini, N, da Paixão, RLDA, Broetto, L, Landell, M, Santi, L, Beys-da-Silva, WO, Silveira, CP, Serrano, TR, de Oliveira, ES, Kmetzsch, L, Vainstein, MH, de Vasconcelos, ATR & Schrank, A 2014, 'Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins', BMC Genomics, vol. 15, pp. 822. https://doi.org/10.1186/1471-2164-15-822

TY - JOUR

T1 - Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins

AU - Staats, Charley Christian

AU - Junges, Angela

AU - Guedes, Rafael Lucas Muniz

AU - Thompson, Claudia Elizabeth

AU - de Morais, Guilherme Loss

AU - Boldo, Juliano Tomazzoni

AU - de Almeida, Luiz Gonzaga Paula

AU - Andreis, Fábio Carrer

AU - Gerber, Alexandra Lehmkuhl

AU - Sbaraini, Nicolau

AU - da Paixão, Rana Louise de Andrade

AU - Broetto, Leonardo

AU - Landell, Melissa

AU - Santi, Lucélia

AU - Beys-da-Silva, Walter Orlando

AU - Silveira, Carolina Pereira

AU - Serrano, Thaiane Rispoli

AU - de Oliveira, Eder Silva

AU - Kmetzsch, Lívia

AU - Vainstein, Marilene Henning

AU - de Vasconcelos, Ana Tereza Ribeiro

AU - Schrank, Augusto

PY - 2014/9/29

Y1 - 2014/9/29

N2 - BACKGROUND: Metarhizium anisopliae is an entomopathogenic fungus used in the biological control of some agricultural insect pests, and efforts are underway to use this fungus in the control of insect-borne human diseases. A large repertoire of proteins must be secreted by M. anisopliae to cope with the various available nutrients as this fungus switches through different lifestyles, i.e., from a saprophytic, to an infectious, to a plant endophytic stage. To further evaluate the predicted secretome of M. anisopliae, we employed genomic and transcriptomic analyses, coupled with phylogenomic analysis, focusing on the identification and characterization of secreted proteins.RESULTS: We determined the M. anisopliae E6 genome sequence and compared this sequence to other entomopathogenic fungi genomes. A robust pipeline was generated to evaluate the predicted secretomes of M. anisopliae and 15 other filamentous fungi, leading to the identification of a core of secreted proteins. Transcriptomic analysis using the tick Rhipicephalus microplus cuticle as an infection model during two periods of infection (48 and 144 h) allowed the identification of several differentially expressed genes. This analysis concluded that a large proportion of the predicted secretome coding genes contained altered transcript levels in the conditions analyzed in this study. In addition, some specific secreted proteins from Metarhizium have an evolutionary history similar to orthologs found in Beauveria/Cordyceps. This similarity suggests that a set of secreted proteins has evolved to participate in entomopathogenicity.CONCLUSIONS: The data presented represents an important step to the characterization of the role of secreted proteins in the virulence and pathogenicity of M. anisopliae.

AB - BACKGROUND: Metarhizium anisopliae is an entomopathogenic fungus used in the biological control of some agricultural insect pests, and efforts are underway to use this fungus in the control of insect-borne human diseases. A large repertoire of proteins must be secreted by M. anisopliae to cope with the various available nutrients as this fungus switches through different lifestyles, i.e., from a saprophytic, to an infectious, to a plant endophytic stage. To further evaluate the predicted secretome of M. anisopliae, we employed genomic and transcriptomic analyses, coupled with phylogenomic analysis, focusing on the identification and characterization of secreted proteins.RESULTS: We determined the M. anisopliae E6 genome sequence and compared this sequence to other entomopathogenic fungi genomes. A robust pipeline was generated to evaluate the predicted secretomes of M. anisopliae and 15 other filamentous fungi, leading to the identification of a core of secreted proteins. Transcriptomic analysis using the tick Rhipicephalus microplus cuticle as an infection model during two periods of infection (48 and 144 h) allowed the identification of several differentially expressed genes. This analysis concluded that a large proportion of the predicted secretome coding genes contained altered transcript levels in the conditions analyzed in this study. In addition, some specific secreted proteins from Metarhizium have an evolutionary history similar to orthologs found in Beauveria/Cordyceps. This similarity suggests that a set of secreted proteins has evolved to participate in entomopathogenicity.CONCLUSIONS: The data presented represents an important step to the characterization of the role of secreted proteins in the virulence and pathogenicity of M. anisopliae.

KW - Animals

KW - Comparative Genomic Hybridization

KW - Fungal Proteins/genetics

KW - Gene Expression Profiling

KW - Genome, Fungal

KW - Host-Pathogen Interactions/genetics

KW - Metarhizium/classification

KW - Phylogeny

KW - Rhipicephalus/metabolism

KW - Sequence Analysis, RNA

U2 - 10.1186/1471-2164-15-822

DO - 10.1186/1471-2164-15-822

M3 - Article

C2 - 25263348

SN - 1471-2164

VL - 15

SP - 822

JO - BMC Genomics

JF - BMC Genomics

ER -

Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins

Abstract

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