Abstract

Prokaryotes represent a source of both biotechnological and pharmaceutical molecules of importance, such as nonribosomal peptides (NRPs). NRPs are secondary metabolites which their synthesis is independent of ribosomes. Traditionally, obtaining NRPs had focused on organisms from terrestrial environments, but in recent years marine and coastal environments have emerged as an important source for the search and obtaining of nonribosomal compounds. In this study, we carried out a metataxonomic analysis of sediment of the coast of Yucatan in order to evaluate the potential of the microbial communities to contain bacteria involved in the synthesis of NRPs in two sites: one contaminated and the other conserved. As well as a metatranscriptomic analysis to discover nonribosomal peptide synthetases (NRPSs) genes. We found that the phyla with the highest representation of NRPs producing organisms were the Proteobacteria and Firmicutes present in the sediments of the conserved site. Similarly, the metatranscriptomic analysis showed that 52% of the sequences identified as catalytic domains of NRPSs were found in the conserved site sample, mostly (82%) belonging to Proteobacteria and Firmicutes; while the representation of Actinobacteria traditionally described as the major producers of secondary metabolites was low. It is important to highlight the prediction of metabolic pathways for siderophores production, as well as the identification of NRPS’s condensation domain in organisms of the Archaea domain. Because this opens the possibility to the search for new nonribosomal structures in these organisms. This is the first mining study using high throughput sequencing technologies conducted in the sediments of the Yucatan coast to search for bacteria producing NRPs, and genes that encode NRPSs enzymes.

Highlights

  • Prokaryotes are the most abundant organisms in coastal and estuarine ecosystems, and their anaerobic respiratory processes contribute to the transformation of nitrogen, sulfur, iron and carbon, playing a key role in the productivity of the coastal marine ecosystem, as well as in the regulation of relevant processes in global biogeochemical cycles [1,2]

  • The condensation domain that performs the synthesis of the antimicobacterial cyclomarin, was identified in an organism belonging to the Crenarchaeota phylum in the sample of El Palmar. This is a very prominent result since it opens the possibility to the search for new structures of NRPs, but in general, it opens the possibility to the search in Archaea for NRPs with new structures not previously described, since the identification of nonribosomal compounds has focused only in certain groups of bacteria. This is the first study in which a systematic analysis of sediments of the wetlands of the Yucatan coast is carried out using next-generation sequencing tools, for the metataxonomic search of bacteria producing nonribosomal peptides

  • From our taxonomic profiles analysis, we have observed that the abundance of bacteria that have traditionally been associated with the production of NRPs, such as Actinobacteria, is low in the coastal sediments of the wetlands of the Yucatan coast

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Summary

Introduction

Prokaryotes are the most abundant organisms in coastal and estuarine ecosystems, and their anaerobic respiratory processes contribute to the transformation of nitrogen, sulfur, iron and carbon, playing a key role in the productivity of the coastal marine ecosystem, as well as in the regulation of relevant processes in global biogeochemical cycles [1,2]. 50% of drugs that are in clinical use belong to the NRPs or mixed polyketide-nonribosomal peptide families derived from natural products isolated from marine bacteria These contribute to 70% of NRPs discovered with the activity of antimicrobial, antiviral, cytostatic, immunosuppressant, antimalarial, antiparasitic, animal growth promoters and natural insecticides [7]. The biosynthesis of the NRPs can be carried out by three types of NRPSs: type A, a linear NRPS in which each enzymatic domain is used once during the biosynthesis; type B, an iterative NRPS that uses all its modules more than once during the biosynthesis; whereas Type C is a non-linear NRPS that work more than once during the biosynthesis of a single NRP [10] These secondary metabolites represent promising scaffolds for the development of new drugs [11] due to the great structural diversity they have, derived from having more than 300 different precursors and are not limited to only 20 proteinogenic amino acids [12]. A metatranscriptomic analysis was carried out to identify genes of catalytic domains present in the NRPSs and the evaluation of their transcriptional expression

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