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Genome Mining As New Challenge in Natural Products Discovery marine drugs Review Genome Mining as New Challenge in Natural Products Discovery 1,2, 1,2, 1 1, Luisa Albarano y, Roberta Esposito y, Nadia Ruocco and Maria Costantini * 1 Department of Marine Biotechnology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy; [email protected] (L.A.); [email protected] (R.E.); [email protected] (N.R.) 2 Department of Biology, University of Naples Federico II, Complesso Universitario di Monte Sant’Angelo, Via Cinthia 21, 80126 Napoli, Italy * Correspondence: [email protected]; Tel.: +39-081-583-3315; Fax: +39-081-764-1355 These authors contributed equally to this work. y Received: 4 March 2020; Accepted: 3 April 2020; Published: 9 April 2020 Abstract: Drug discovery is based on bioactivity screening of natural sources, traditionally represented by bacteria fungi and plants. Bioactive natural products and their secondary metabolites have represented the main source for new therapeutic agents, used as drug leads for new antibiotics and anticancer agents. After the discovery of the first biosynthetic genes in the last decades, the researchers had in their hands the tool to understand the biosynthetic logic and genetic basis leading to the production of these compounds. Furthermore, in the genomic era, in which the number of available genomes is increasing, genome mining joined to synthetic biology are offering a significant help in drug discovery. In the present review we discuss the importance of genome mining and synthetic biology approaches to identify new natural products, also underlining considering the possible advantages and disadvantages of this technique. Moreover, we debate the associated techniques that can be applied following to genome mining for validation of data. Finally, we review on the literature describing all novel natural drugs isolated from bacteria, fungi, and other living organisms, not only from the marine environment, by a genome-mining approach, focusing on the literature available in the last ten years. Keywords: bacteria; fungi; genome mining; natural products; synthetic biology 1. Introduction on Bioactive Natural Products Isolation Nature is an important source of bioactive products and their derivatives (secondary metabolites), which form part of many important drugs formation widely used in the clinic field [1]. In fact, as reported in Newman and Cragg [2], over the last 30 years the great majority of anticancer, anti-infective, and anti-bacterial drugs are represented by natural products and their derivatives, produced by all organisms (from bacteria to plants, invertebrate, and other animals) with different chemical structure and leading to several biological activities [3,4]. Furthermore, these secondary metabolites have influenced the development of several drugs, including antibacterial, anticancer, and anti-cholesterol agents [5]. Several of these bioactive products are derived from microorganisms, such as fungi and bacteria [6], which have represented an important source of antibiotics and many other medicines [7,8]. In particular many bacteria deriving from the marine environment, particularly those found in association with marine invertebrates (such as sponges), are able to produce secondary metabolites with potential anticancer and antifungal roles because of their cytotoxic properties [9,10]. Considering the great problem of the antimicrobial resistance increase and its high impact on human health, there is an important need of searching for new natural products that could therefore remedy this issue [11,12]. For these reasons, in the past decade, genomic science has been used to identify the possible drug Mar. Drugs 2020, 18, 199; doi:10.3390/md18040199 www.mdpi.com/journal/marinedrugs Mar. Drugs 2020, 18, 199 2 of 17 Mar. Drugs 2020, 18, x 2 of 17 developmenttargets and to of find the novel genome genes sequencing cluster for technologies the biosynthesis to find of naturalnovel metabolites products [13 has]. Thesurely development drown the attentionof the genome of pharmaceutical sequencing technologies industries, which to find had novel by now metabolites lost interest has in surely natural drown products the attention due to the of pharmaceuticaladvent of combinatorial industries, chemistry which had [14]. by now The lost advent interest of inbased-genome natural products sequencing due to the techniques, advent of especiallycombinatorial with chemistry establishment [14]. of The genome advent mining, of based-genome has allowed sequencing to obtain new techniques, natural drugs especially in a faster with andestablishment cheaper way. of genome mining, has allowed to obtain new natural drugs in a faster and cheaper way. 1.1.Genome Genome Mining Mining The term “genome“genome mining”mining” are are associated associated to to every every bioinformatics bioinformatics investigation investigation used used to detect to detect not notonly only the biosyntheticthe biosynthetic pathway pathway of bioactive of bioactive natural natu products,ral products, but alsobut also their their possible possible functional functional and andchemical chemical interactions interactions [15]. Specifically,[15]. Specifically, the genome the genome mining involvesmining theinvolves identification the identification of previously of previouslyuncharacterized uncharacterized natural product natural biosynthetic product gene biosyn clustersthetic within gene the clusters genomes within of sequenced the genomes organisms, of sequencedsequence analysis organisms, of the sequence enzymes analysis encoded of bythe these enzymes gene encoded clusters, by together these gene with clusters, the experimental together withidentification the experimental of the products identification of the geneof the clusters products (Figure of the1;[ gene16]). clusters (Figure 1; [16]). Figure 1. AssociatedAssociated techniques techniques (categorized (categorized as as molecular biology techniques, chemical analysis, cellular biology techniques, and and bioinformatic analys analysis)is) to to genome genome mining mining fo forr validation validation of of data, data, leading together to drug discovery. Genome mining is entirely dependent on computin computingg technology and bioinformaticsbioinformatics tools. About this point, a huge amount of data, consisting of DNA sequences and their annotations, are now deposited in publicly accessible databases. The The st storageorage and and handling of these resources relies on the continued development development of of computers computers and and the the networ networks.ks. Once Once all allthe the genes genes within within a new a new genome genome are identified,are identified, they they can canbe compared be compared with with those those of kn ofown known functions functions in the in public the public databases. databases. Both Bothraw andraw andannotated annotated genomic genomic data, data, as we as wellll as asbioinformatics bioinformatics tools, tools, for for sequence sequence comparisons comparisons are are freely freely available through the didifferentfferent websites.websites. It also important to keep in mind that it is now a mandatory publication prerequisite of most scientificscientific journals that sequence data from research involving novel DNA sequences is deposited in a publicly accessible database. In the case for which which the the sequences sequences of of many many prot proteins,eins, encoding for enzymes, involved in natural product biosynthesis are deposited in these databases, it is relatively easy to identify pathways in which theythey areare involvedinvolved by by sequence sequence comparisons. comparisons. The The availability availability of of these these synthesis synthesis enzymes enzymes and and the pathwaysthe pathways in which in which they they operate, operate, together together with with the sequencethe sequence comparisons comparisons with with genes genes from from which which they theyarise, arise, can certainly can certainly be used be to used identify to identify homologs, homologs, and potentially and potentially the pathways, the pathways, in the new in organismthe new organismunder analysis. under However, analysis. itHowever, is important it is to important consider thatto consider many enzymes that many are similarenzymes in sequencesare similar but in sequences but follow chemical processes that are slightly different, leading to a different pathway or very different final end product. Mar. Drugs 2020, 18, 199 3 of 17 follow chemical processes that are slightly different, leading to a different pathway or very different final end product. Furthermore, genome mining has a strong support by synthetic biology, consisting in the design and the construction of new biological, as for examples enzymes, genetic circuits and/or the redesign of existing biological systems. These combined approaches are mainly used to detect novel natural products in bacteria and fungi probably because of operon organization of their synthesis genes [13], allowing the control of transcriptional levels and also the association of their potential metabolic function [17]. Moreover, the central role of genome mining consists in finding new biosynthetic gene clusters (BGCs). In fact, the BGCs encode for two class of enzymes, polyketide synthases (PKS) and non-ribosomal peptide synthases (NRPS), which are the two most important biosynthetic routes responsible for the formation of natural products [18]. This approach also provides the possibility to compare target gene clusters to known gene clusters
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