Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species
IntroductionTheobroma cacao, the cocoa tree, is a target for pathogens, such as fungi from the genera Phytophthora, Moniliophthora, Colletotrichum, Ceratocystis, among others. Some cacao pathogens are restricted to specific regions of the world, such as the Cacao swollen shoot virus (CSSV) in West A...
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1053562/full |
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| author | Brayan Maudiel Diaz Reyes Paula Luize Camargos Fonseca Paula Luize Camargos Fonseca Neander Marcel Heming Lucas Barbosa de Amorim Conceição Katiucia Ticila de Souza Nascimento Karina Peres Gramacho Enrique Arevalo-Gardini Enrique Arevalo-Gardini Carlos Priminho Pirovani Eric Roberto Guimarães Rocha Aguiar |
| author_facet | Brayan Maudiel Diaz Reyes Paula Luize Camargos Fonseca Paula Luize Camargos Fonseca Neander Marcel Heming Lucas Barbosa de Amorim Conceição Katiucia Ticila de Souza Nascimento Karina Peres Gramacho Enrique Arevalo-Gardini Enrique Arevalo-Gardini Carlos Priminho Pirovani Eric Roberto Guimarães Rocha Aguiar |
| author_sort | Brayan Maudiel Diaz Reyes |
| collection | DOAJ |
| description | IntroductionTheobroma cacao, the cocoa tree, is a target for pathogens, such as fungi from the genera Phytophthora, Moniliophthora, Colletotrichum, Ceratocystis, among others. Some cacao pathogens are restricted to specific regions of the world, such as the Cacao swollen shoot virus (CSSV) in West African countries, while others are expanding geographically, such as Moniliophthora roreri in the Americas. M. roreri is one of the most threatening cacao pathogens since it directly attacks the cacao pods driving a significant reduction in production, and therefore economic losses. Despite its importance, the knowledge about the microenvironment of this pathogen and the cocoa pods is still poorly characterized.MethodsHerein we performed RNA sequencing of spores in differential stages of culture in a medium supplemented with cacao pod extract and mycelium collected of the susceptible variety ICT 7121 naturally infected by the pathogen to evaluate the diversity and transcriptional activity of microorganisms associated with the in vitro sporulation of M. roreri.ResultsOur data revealed a great variety of fungi and bacteria associated with M. roreri, with an exceptional diversity of individuals from the genus Trichoderma sp. Interestingly, the dynamics of microorganisms from different kingdoms varied proportionally, suggesting they are somehow affected by M. roreri culture time. We also identified three sequences similar to viral genomes from the Narnaviridae family, posteriorly confirmed by phylogenetic analysis as members of the genus Narnavirus. Screening of M. roreri public datasets indicated the virus sequences circulating in samples from Ecuador, suggesting a wide spread of these elements. Of note, we did not identify traces of the viral sequences in the M. roreri genome or DNA sequencing, restricting the possibility of these sequences representing endogenized elements.DiscussionTo the best of our knowledge, this is the first report of viruses infecting the fungus of the genus Moniliophthora and only the third description of viruses that are able to parasite elements from the Marasmiaceae family. |
| first_indexed | 2024-04-10T17:40:26Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-10T17:40:26Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-d09928d4dc2f4084be780a4503ca3b052023-02-03T15:28:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011310.3389/fmicb.2022.10535621053562Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral speciesBrayan Maudiel Diaz Reyes0Paula Luize Camargos Fonseca1Paula Luize Camargos Fonseca2Neander Marcel Heming3Lucas Barbosa de Amorim Conceição4Katiucia Ticila de Souza Nascimento5Karina Peres Gramacho6Enrique Arevalo-Gardini7Enrique Arevalo-Gardini8Carlos Priminho Pirovani9Eric Roberto Guimarães Rocha Aguiar10Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilDepartamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilDepartamento de Genética, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilInstituto de Biologia, Universidade Federal da Bahia, Salvador, BrazilDepartamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilCentro de Pesquisas do Cacau, Comissão Executivo do Plano da Lavoura Cacaueira, CEPEC/CEPLAC, Rodovia Ilhéus-Itabuna, Ilhéus, BrazilInstituto de Cultivos Tropicales, Tarapoto, PeruUniversidad Nacional Autónoma de Alto Amazonas, Yurimaguas, PeruDepartamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilDepartamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BrazilIntroductionTheobroma cacao, the cocoa tree, is a target for pathogens, such as fungi from the genera Phytophthora, Moniliophthora, Colletotrichum, Ceratocystis, among others. Some cacao pathogens are restricted to specific regions of the world, such as the Cacao swollen shoot virus (CSSV) in West African countries, while others are expanding geographically, such as Moniliophthora roreri in the Americas. M. roreri is one of the most threatening cacao pathogens since it directly attacks the cacao pods driving a significant reduction in production, and therefore economic losses. Despite its importance, the knowledge about the microenvironment of this pathogen and the cocoa pods is still poorly characterized.MethodsHerein we performed RNA sequencing of spores in differential stages of culture in a medium supplemented with cacao pod extract and mycelium collected of the susceptible variety ICT 7121 naturally infected by the pathogen to evaluate the diversity and transcriptional activity of microorganisms associated with the in vitro sporulation of M. roreri.ResultsOur data revealed a great variety of fungi and bacteria associated with M. roreri, with an exceptional diversity of individuals from the genus Trichoderma sp. Interestingly, the dynamics of microorganisms from different kingdoms varied proportionally, suggesting they are somehow affected by M. roreri culture time. We also identified three sequences similar to viral genomes from the Narnaviridae family, posteriorly confirmed by phylogenetic analysis as members of the genus Narnavirus. Screening of M. roreri public datasets indicated the virus sequences circulating in samples from Ecuador, suggesting a wide spread of these elements. Of note, we did not identify traces of the viral sequences in the M. roreri genome or DNA sequencing, restricting the possibility of these sequences representing endogenized elements.DiscussionTo the best of our knowledge, this is the first report of viruses infecting the fungus of the genus Moniliophthora and only the third description of viruses that are able to parasite elements from the Marasmiaceae family.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1053562/fullTheobroma cacaomicrobiotametatranscriptomicsfrosty pod rot diseasevirusnarnavirus |
| spellingShingle | Brayan Maudiel Diaz Reyes Paula Luize Camargos Fonseca Paula Luize Camargos Fonseca Neander Marcel Heming Lucas Barbosa de Amorim Conceição Katiucia Ticila de Souza Nascimento Karina Peres Gramacho Enrique Arevalo-Gardini Enrique Arevalo-Gardini Carlos Priminho Pirovani Eric Roberto Guimarães Rocha Aguiar Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species Frontiers in Microbiology Theobroma cacao microbiota metatranscriptomics frosty pod rot disease virus narnavirus |
| title | Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species |
| title_full | Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species |
| title_fullStr | Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species |
| title_full_unstemmed | Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species |
| title_short | Characterization of the microbiota dynamics associated with Moniliophthora roreri, causal agent of cocoa frosty pod rot disease, reveals new viral species |
| title_sort | characterization of the microbiota dynamics associated with moniliophthora roreri causal agent of cocoa frosty pod rot disease reveals new viral species |
| topic | Theobroma cacao microbiota metatranscriptomics frosty pod rot disease virus narnavirus |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1053562/full |
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