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Marine Microbiome As Source of Natural Products bs_bs_banner doi:10.1111/1751-7915.12882 Editorial: The microbiome as a source of new enterprises and job creation Marine microbiome as source of natural products Fernando de la Calle Department of Microbiology R&D, Pharma Mar S.A., Avda. de los Reyes, 1. Colmenar Viejo, 28770 Madrid, Spain. Less than 1% of living microorganisms can be cultured bioenergy and algal cosmetics and underestimate the in the laboratory, but even this minute part has produced role of the marine microbiome. Market opportunities and incredible discoveries such as antibiotics that have job creation are likely to significantly increase in the saved millions of lifes. We can only imagine what other future with the advent of transversal technologies direc- great inventions will come to light when the rest of this ted at exploiting other biotechnological advances, such enormous universe of living genomes is awakened. as the evolution of bioinformatics, synthetic biology, Everything is recorded in the genes, and modern molecular diagnostics and devices, biocatalysis and the metagenomic studies, involving the large-scale sequenc- many OMICS technologies. The marine microbiome ing of the genetic material of marine microorganisms, as must be an essential part of the bioeconomy. However, well as the similarities between the human gut and whilst the enormous potential of the marine microbiome ocean microbiomes, are not only providing powerful has been recognized by industry, there is currently a insights into why the Earth is a living planet, but are also lack of coordination amongst policy makers, govern- revealing possible causes and promising cures for meta- ments, civil society organizations, academia and large bolic diseases, including cancer. The marine microbiome industries, perhaps due in part to the reluctance of big contains many billions of genes with the ability to companies to invest in innovations for the long term. express an unimaginable arsenal of small molecules, as This scenario represents an excellent opportunity to cre- well as proteins, lipids and others classes of products ate small- and medium-sized enterprises that are highly with ecological functions that can be ‘humanized’ for the specialized. A new wave of such ‘marine biotech enter- discovery of new pharmaceuticals, improved enzymes, prises’ based on modern bioprospecting would provide biopolymers and novel biomaterials, as well as new employment for highly qualified staff and the chance to resources for food and feed stocks, nutraceuticals, diag- pursue innovative, ‘high-tech’ ideas at the cutting edge nostic devices, personal care and cosmetic products and of modern science. an ever-increasing list of marine natural products. Today, The complexity of the human gut microbiome has lim- the term Marine Biodiversity is known as Marine Geno- ited the development of microbiome-based therapeutics mic Resources. (Van der Lelie et al., 2017). However, this could be an Whilst ‘Blue Biotechnology’ remains in its infancy, a excellent opportunity to improve current technologies to report for European DG Maritime Affairs and Fisheries further understand the term ‘microbiome complexity’ and (2014) (http://ec.europa.eu/dgs/maritimeaffairs_fisheries/ create a new network of innovative enterprises and fur- consultations/index_en.htm) projected that revenue in ther job opportunities. Metagenome approaches, includ- Europe from blue biotechnology could reach €1 billion ing next-generation gene sequencing, bioinformatics, within 5 years if a market growth of 6–8% per annum functional genomics, transcriptomics, metabolomics and was maintained and result in creation of 10 000 new other OMICS technologies, including the efficient engi- jobs. A 2015 report analysis of market for marine neering of bacteria chassis for heterologous expression biotechnology from Smithers Rapra (http://www.smithe as well as knowledge of cell-to-cell communication are rsrapra.com/news/2015/October/market-for-marine-biotec all transversal disciplines that can be used outside the hnology) indicated that this global market has the poten- realm of the human body to interpret the role of other tial to reach $4.8 billion by 2020, rising to $6.4 billion by global microbiomes, including the marine microbiome. 2025. However, in the main, these estimations are The bacterial habitants of the human gut may control based on ‘classical’ approaches such as aquaculture, the health of our immune system, but the marine ª 2017 The Author. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1294 Editorial microbiome manages the health of life on earth, including led to the isolation of several classes of bioactive natural the biogeological balances mitigating climate changes. products that were mainly small molecules such as But what really is the marine microbiome? polyketides and non-ribosomal peptides. However, there The concept of microbial communities in the marine is an increasing foundation for the rational suspicion, environment has gained increasing importance over the based on marine sponge/tunicate metagenomics, that last few decades due to the abundance of living forms, such compounds although originally isolated from meta- their diversity and the critical role of the marine micro- zoan organisms are in actual fact of bacterial origin. biome in determining the structure and function of There are now many cases of molecules such as tra- oceans, and as a key player in the regulation of the car- bectedin, didemnins, onnamides, bryostatin, dolastatin, bon and nitrogen cycles and the balance of the global swinholides, calyculin A and other fascinating marine marine biomass. Some highlights from the Census of compounds where the putative gene clusters have been Marine Life (2010) (http://www.coml.org/) has revealed identified in symbionts or free-living bacteria, thereby the astonishing fact that the number of bacteria in the confirming the role of the marine microbiome as a pro- open ocean exceeds 1029, representing more than 90% ducer of bioactive metabolites with potential applications of the total marine biomass, with more than one million in oncology. The paper of Wilson et al. (2014) is highly living bacteria in each millilitre of sea water. A single litre recommended and describes how they have identified a of seawater has been estimated to contain approxi- bacterial symbiont, living in sponges and harbouring a mately 20 000 species with archaeal cell numbers rival- large number of gene clusters for secondary metabolites. ling those of bacteria as well as an astronomic number The type of chemical scaffold produced is not restricted of eukaryotic cells and marine viruses and phages. In to anticancer bioactives, and other polyketide and pep- reality, nobody actually knows how many bacteria, tide small molecules are continuously being discovered archaea or eukaryotic microorganisms and viruses are as anti-infective or modulation agents for metabolic currently living or would be able to survive in the ocean’s diseases. dark depths. This question may remain unanswered for Currently, genomic mining for polyketide synthases many decades. (PKS) and non-ribosomal peptide synthetases (NRPS) This fascinating universe of different life forms is far improves the probability of success in drug discovery from being a collection of static elements, but is continu- using marine microorganisms, both in isolated genomes ously interacting amongst themselves and with their and metagenomes. Over recent years, several computa- environment, developing strategies for survival beyond tional tools have been developed for the analysis and the wildest imagination of our rational human minds. prediction of specific classes of secondary metabolites. Evolution has developed a myriad of enzymatic reactions AntiSMASH (Blin et al., 2017) has served as a compre- and highly selective chemical weapons in response to hensive web server and a stand-alone tool for the auto- quorum sensing signals. This adds an extra level of matic genomic identification and analysis of biosynthetic complexity to the understanding of the marine micro- gene clusters of any type, with other more specific tools biome. such as ClustScan, NP.searcher or SBSPKS focusing An example of successful ‘blue business’ that provides on non-ribosomal peptide and polyketide biosynthesis ‘proof-of-concept’ for exploiting marine chemical diversity pathways. Such bioinformatic tools are creating great in human health is demonstrated by the approval of the expectations for future drug discovery by revealing the marine-derived medicine Yondelisâ (trabectedin) for the multitude of silent (cryptic) biosynthetic gene clusters. treatment of certain types of soft tissue sarcomas and In parallel, ever-increasing research efforts are being ovarian cancers. This compound has been developed by directed towards personal care products based on mar- PharmaMar, a biopharmaceutical company focused on ine microbial components. Cosmeceuticals, the combina- oncology and committed to research and development tion of cosmetics and pharmaceuticals, is a booming and taking inspiration from the sea to discover molecules business and revenues for this sector are expected to with antitumor activity. Trabectedin belongs to the ectei- show two-digit growth over the next few decades. The nascidin family
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