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The Unexplored Wealth of Microbial Secondary Metabolites: the Sphingobacteriaceae Case Study

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Abstract

Research on secondary metabolites (SMs) has been mostly focused on Gram-positive bacteria, especially Actinobacteria. The association of genomics with robust bioinformatics tools revealed the neglected potential of Gram-negative bacteria as promising sources of new SMs. The family Sphingobacteriaceae belongs to the phylum Bacteroidetes having representatives in practically all environments including humans, rhizosphere, soils, wastewaters, among others. Some genera of this family have demonstrated great potential as plant growth promoters, bioremediators and producers of some value-added compounds such as carotenoids and antimicrobials. However, to date, Sphingobacteriaceae’s SMs are still poorly characterized, and likewise, little is known about their chemistry. This study revealed that Sphingobacteriaceae pangenome encodes a total of 446 biosynthetic gene clusters (BGCs), which are distributed across 85 strains, highlighting the great potential of this bacterial family to produce SMs. Pedobacter, Mucilaginibacter and Sphingobacterium were the genera with the highest number of BGCs, especially those encoding the biosynthesis of ribosomally synthesized and post-translationally modified peptides (RiPPs), terpenes, polyketides and nonribosomal peptides (NRPs). In Mucilaginibacter and Sphingobacterium genera, M. lappiensis ATCC BAA-1855, Mucilaginibacter sp. OK098 (both with 11 BGCs) and Sphingobacterium sp. 21 (6 BGCs) are the strains with the highest number of BGCs. Most of the BGCs found in these two genera did not have significant hits with the MIBiG database. These results strongly suggest that the bioactivities and environmental functions of these compounds, especially RiPPs, PKs and NRPs, are still unknown. Among RiPPs, two genera encoded the production of class I and class III lanthipeptides. The last are associated with LanKC proteins bearing uncommon lyase domains, whose dehydration mechanism deserves further investigation. This study translated genomics into functional information that unveils the enormous potential of environmental Gram-negative bacteria to produce metabolites with unknown chemistries, bioactivities and, more importantly, unknown ecological roles.

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Data Availability

All the data is available in open access genomic databases.

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The codes of all the software applied in this study are available.

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Acknowledgements

We are thankful to Dr. Jorge Navarro-Muñoz for his help, which allowed us to run BiG-SCAPE software package properly.

Funding

Cláudia Covas was supported by Fundação para a Ciência e Tecnologia (FCT), POPH and European Union grant SFRH/BD/98446/2013. Tânia Caetano was funded by national funds (OE), through FCT in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July (CEECIND/01463/2017).

The CESAM research unit is supported by FCT/MCTES through national funds (UIDP/50,017/2020 + UIDB/50,017/2020).

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  1. Gonçalo Figueiredo and Margarida Gomes contributed equally to this work.

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  1. CESAM and Department of Biology, University of Aveiro, 3810-193, Aveiro, Portugal

    Gonçalo Figueiredo, Margarida Gomes, Claúdia Covas, Sónia Mendo & Tânia Caetano

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  3. Claúdia Covas
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Contributions

Conceptualization: Tania Caetano, Claúdia Covas. Data curation: Gonçalo Figueiredo, Margarida Gomes. Formal Analysis: Gonçalo Figueiredo, Margarida Gomes, Claúdia Covas. Investigation: Gonçalo Figueiredo, Margarida Gomes, Claúdia Covas. Supervision: Tania Caetano, Sónia Mendo. Writing — original draft: Gonçalo Figueiredo, Margarida Gomes, Claúdia Covas, Sónia Mendo, Tânia Caetano. Writing — review & editing: Gonçalo Figueiredo, Margarida Gomes, Claúdia Covas, Sónia Mendo, Tânia Caetano.

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Correspondence to Tânia Caetano.

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Figueiredo, G., Gomes, M., Covas, C. et al. The Unexplored Wealth of Microbial Secondary Metabolites: the Sphingobacteriaceae Case Study. Microb Ecol 83, 470–481 (2022). https://doi.org/10.1007/s00248-021-01762-3

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