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Evolutionary genomics and biosynthetic potential of novel environmental Actinobacteria

  • Genomics, Transcriptomics, Proteomics
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Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Actinobacteria embroil Gram-positive microbes with high guanine and cytosine contents in their DNA. They are the source of most antimicrobials of bacterial origin utilized in medicine today. Their genomes are among the richest in novel secondary metabolites with high biotechnological potential. Actinobacteria reveal complex patterns of evolution, responses, and adaptations to their environment, which are not yet well understood. We analyzed three novel plant isolates and explored their habitat adaptation, evolutionary patterns, and potential secondary metabolite production. The phylogenomically characterized isolates belonged to Actinoplanes sp. TFC3, Streptomyces sp. L06, and Embleya sp. NF3. Positively selected genes, relevant in strain evolution, encoded enzymes for stress resistance in all strains, including porphyrin, chlorophyll, and ubiquinone biosynthesis in Embleya sp. NF3. Streptomyces sp. L06 encoded for pantothenate and proteins for CoA biosynthesis with evidence of positive selection; furthermore, Actinoplanes sp. TFC3 encoded for a c-di-GMP synthetase, with adaptive mutations. Notably, the genomes harbored many genes involved in the biosynthesis of at least ten novel secondary metabolites, with many avenues for future new bioactive compound characterization—specifically, Streptomyces sp. L06 could make new ribosomally synthesized and post-translationally modified peptides, while Embleya sp. NF3 could produce new non-ribosomal peptide synthetases and ribosomally synthesized and post-translationally modified peptides. At the same time, TFC3 has particularly enriched in terpene and polyketide synthases. All the strains harbored conserved genes in response to diverse environmental stresses, plant growth promotion factors, and degradation of various carbohydrates, which supported their endophytic lifestyle and showed their capacity to colonize other niches. This study aims to provide a comprehensive estimation of the genomic features of novel Actinobacteria. It sets the groundwork for future research into experimental tests with new bioactive metabolites with potential application in medicine, biofertilizers, and plant biomass residue utilization, with potential application in medicine, as biofertilizers and in plant biomass residues utilization.

Key points

Potential of novel environmental bacteria for secondary metabolites production

Exploring the genomes of three novel endophytes isolated from a medicinal tree

Pan-genome analysis of Actinobacteria genera

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Data availability

The genomes reported in this manuscript were deposited at GenBank under the accession JACBNV00000000 for Streptomyces sp. L06 https://www.ncbi.nlm.nih.gov/nuccore/JACBNV000000000.1/. The accession numbers for the genome sequences used for comparison with the novel genomes are included in the Table S1 of the manuscript.

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Acknowledgements

CCM thanks MINCIENCIAS-Colombia for the awarded scholarship. MPGR is involved in the MSc program of Biochemical Sciences from the Universidad Nacional Autónoma de México and was supported by the postgraduate fellowship 749456 from CONACYT, Mexico. SS acknowledges the economic support from DGAPA, PAPIIT IN-205519, IN-205922, and CONACYT A-S1-9143. The support of the NUATEI program from Instituto de Investigaciones Biomédicas, UNAM is also recognized. We thank Marco A. Ortiz-Jiménez for strain preservation studies and Dr. Beatriz Ruiz-Villafán for her assistance during this work edition.

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Contributions

CCM and MPGR performed all the bioinformatics analyses. CCM, MPGR RAMR, SDRL, and SS contributed to the conception and wrote the manuscript sections. MVH executed DNA extraction, DNA sequencing, and genome assembly. SS and RRS revised, read, edited, and approved the final version of the manuscript.

Corresponding author

Correspondence to Sergio Sanchez.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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The authors declare no conflict of interest.

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Caicedo-Montoya, C., Gómez-Román, M.P., Vázquez-Hernández, M. et al. Evolutionary genomics and biosynthetic potential of novel environmental Actinobacteria. Appl Microbiol Biotechnol 105, 8805–8822 (2021). https://doi.org/10.1007/s00253-021-11659-3

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  • DOI: https://doi.org/10.1007/s00253-021-11659-3

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