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The Bacterial and Fungal Microbiota of the Mexican Rubiaceae Family Medicinal Plant Bouvardia ternifolia

Abstract

Bouvardia ternifolia is a medicinal plant considered a source of therapeutic compounds, like the antitumoral cyclohexapeptide bouvardin. It is known that large number of secondary metabolites produced by plants results from the interaction of the host and adjacent or embedded microorganisms. Using high-throughput DNA sequencing of V3-16S and V5-18S ribosomal gene libraries, we characterized the endophytic, endophytic + epiphyte bacterial, and fungal communities associated to flowers, leaves, stems, and roots, as well as the rhizosphere. The Proteobacteria (average 80.7%) and Actinobacteria (average 14.7%) were the most abundant bacterial phyla, while Leotiomycetes (average 54.8%) and Dothideomycetes (average 27.4%) were the most abundant fungal classes. Differential abundance for the bacterial endophyte group showed a predominance of Erwinia, Propionibacterium, and Microbacterium genera, while Sclerotinia, Coccomyces, and Calycina genera predominated for fungi. The predictive metagenome analysis for bacteria showed significative abundance of pathways for secondary metabolite production, while a FUNguild analysis revealed the presence of pathotroph, symbiotroph, and saprotrophs in the fungal community. Intra and inter copresence and mutual exclusion interactions were identified for bacterial and fungal kingdoms in the endophyte communities. This work provides a description of the diversity and composition of bacterial and fungal microorganisms living in flowers, leaves, stems, roots, and the rhizosphere of this medicinal plant; thus, it paves the way towards an integral understanding in the production of therapeutic metabolites.

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source of the endophytes. Asterisks indicate taxa with similar abundance: g_Sphingomonas*, Sphingomonas wittichii species; g_Aureobasidium**, Aureobasidium pullulans; g_Sclerotinia***, Sclerotinia trifoliorum; and g_Cladosporium****, Cladosporium albugolaibachiiNc14. Absolute counts are in Supplementary Table S6

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Fig. 6

Availability of Data and Material

The sequence and corresponding mapping files for all samples used in this study were deposited in the NCBI BioSample repository (accession number: PRJNA703940), https://www.ncbi.nlm.nih.gov/sra/PRJNA703940.

Code availability

Not applicable.

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Acknowledgements

We thank CONACyT Doctoral Fellowships for LEV-F (336296) and FH-Q (291236. We are grateful to Rodrigo García-Gutiérrez and Antonia López-Salazar for excellent technical support and Viridiana Rosas-Ocegueda for administrative assistance. We thank Rosa María Pineda Mendoza and Raquel Galvan Villanueva (ENCB-IPN) for technical support on plant taxonomic identification. We recognize the support of the B. Sc. summer students Isabel Montserrat-Cortez de la Puente (2015) and Mariana Román-Reyes (2016) for the development of this work. Jaime García-Mena (19815) is a Fellow from the Sistema Nacional de Investigadores (Mexico).

Funding

This work was financed by the Cinvestav, FONCICYT 2 267416, CONACYT-BMBF-267416 for RS and JGM and CONACyT-163235 INFR-2011–01 for JGM.

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Conceptualization: Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Methods: Loan Edel Villalobos-Flores, Samuel David Espinosa-Torres, Alberto Piña-Escobedo, and Yair Cruz-Narváez. Software: Loan Edel Villalobos-Flores and Fernando Hernández-Quiroz. Validation: Loan Edel Villalobos-Flores and Jaime García-Mena. Formal analysis and investigation: Loan Edel Villalobos-Flores, Fernando Hernández-Quiroz, Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Data curation: Loan Edel Villalobos-Flores, Samuel David Espinosa-Torres, and Jaime García-Mena. Writing—original draft preparation: Loan Edel Villalobos-Flores and Jaime García-Mena. Writing—review and editing: Loan Edel Villalobos-Flores, Yair Cruz-Narváez, Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Visualization: Loan Edel Villalobos-Flores. Funding acquisition: Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Resources: Yair Cruz-Narváez and Jaime García-Mena. Supervision: Jaime García-Mena. Project administration: Jaime García-Mena.

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Correspondence to Jaime García-Mena.

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Villalobos-Flores, L.E., Espinosa-Torres, S.D., Hernández-Quiroz, F. et al. The Bacterial and Fungal Microbiota of the Mexican Rubiaceae Family Medicinal Plant Bouvardia ternifolia. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01871-z

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Keywords

  • Plant endophytes
  • Next-generation DNA sequencing
  • Bouvardin
  • Bacterial-fungal interactions
  • Rhizosphere