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      The Madeira Archipelago As a Significant Source of Marine-Derived Actinomycete Diversity with Anticancer and Antimicrobial Potential

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          Abstract

          Marine-derived actinomycetes have demonstrated an ability to produce novel compounds with medically relevant biological activity. Studying the diversity and biogeographical patterns of marine actinomycetes offers an opportunity to identify genera that are under environmental pressures, which may drive adaptations that yield specific biosynthetic capabilities. The present study describes research efforts to explore regions of the Atlantic Ocean, specifically around the Madeira Archipelago, where knowledge of the indigenous actinomycete diversity is scarce. A total of 400 actinomycetes were isolated, sequenced, and screened for antimicrobial and anticancer activities. The three most abundant genera identified were Streptomyces, Actinomadura, and Micromonospora. Phylogenetic analyses of the marine OTUs isolated indicated that the Madeira Archipelago is a new source of actinomycetes adapted to life in the ocean. Phylogenetic differences between offshore (>100 m from shore) and nearshore (< 100 m from shore) populations illustrates the importance of sampling offshore in order to isolate new and diverse bacterial strains. Novel phylotypes from chemically rich marine actinomycete groups like MAR4 and the genus Salinispora were isolated. Anticancer and antimicrobial assays identified Streptomyces, Micromonospora, and Salinispora as the most biologically active genera. This study illustrates the importance of bioprospecting efforts at unexplored regions of the ocean to recover bacterial strains with the potential to produce novel and interesting chemistry.

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          Most cited references37

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          Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia.

          The culturability of bacteria in the bulk soil of an Australian pasture was investigated by using nutrient broth at 1/100 of its normal concentration (dilute nutrient broth [DNB]) as the growth medium. Three-tube most-probable-number serial dilution culture resulted in a mean viable count that was only 1.4% of the mean microscopically determined total cell count. Plate counts with DNB solidified with agar and with gellan gum resulted in viable counts that were 5.2 and 7.5% of the mean microscopically determined total cell count, respectively. Prior homogenization of the soil sample with an ultrasonic probe increased the viable count obtained by using DNB solidified with gellan gum to 14.1% of the mean microscopically determined cell count. A microscopic examination of the cell aggregates that remained after sonication revealed that the potential CFU count was only 70.4% of the total cell count, due to cells occurring as pairs or in clumps of three or more cells. Staining with SYTO 9 plus propidium iodide indicated that 91.3% of the cells in sonicated soil samples were potentially viable. Together, these findings suggest that the maximum achievable CFU count may be as low as 64.3% of the total cell count. Thirty isolates obtained from plate counting experiments performed with DNB as the growth medium were identified by comparative analysis of partial 16S rRNA gene sequences. A large proportion of these isolates represent the first known isolates of globally distributed groups of soil bacteria belonging to novel lineages within the divisions Actinobacteria, Acidobacteria, Proteobacteria, and Verrucomicrobia.
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            Global patterns in the biogeography of bacterial taxa.

            Bacteria control major nutrient cycles and directly influence plant, animal and human health. However, we know relatively little about the forces shaping their large-scale ecological ranges. Here, we reveal patterns in the distribution of individual bacterial taxa at multiple levels of phylogenetic resolution within and between Earth's major habitat types. Our analyses suggest that while macro-scale habitats structure bacterial distribution to some degree, abundant bacteria (i.e. detectable using 16S rRNA gene sequencing methods) are confined to single assemblages. Additionally, we show that the most cosmopolitan taxa are also the most abundant in individual assemblages. These results add to the growing body of data that support that the diversity of the overall bacterial metagenome is tremendous. The mechanisms governing microbial distribution remain poorly understood, but our analyses provide a framework with which to test the importance of macro-ecological environmental gradients, relative abundance, neutral processes and the ecological strategies of individual taxa in structuring microbial communities. © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd.
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              Marine actinomycetes: an ongoing source of novel bioactive metabolites.

              Actinomycetes are virtually unlimited sources of novel compounds with many therapeutic applications and hold a prominent position due to their diversity and proven ability to produce novel bioactive compounds. There are more than 22,000 known microbial secondary metabolites, 70% of which are produced by actinomycetes, 20% from fungi, 7% from Bacillus spp. and 1-2% by other bacteria. Among the actinomycetes, streptomycetes group are considered economically important because out of the approximately more than 10,000 known antibiotics, 50-55% are produced by this genus. The ecological role of actinomycetes in the marine ecosystem is largely neglected and various assumptions meant there was little incentive to isolate marine strains for search and discovery of new drugs. The search for and discovery of rare and new actinomycetes is of significant interest to drug discovery due to a growing need for the development of new and potent therapeutic agents. Modern molecular technologies are adding strength to the target-directed search for detection and isolation of bioactive actinomycetes, and continued development of improved cultivation methods and molecular technologies for accessing the marine environment promises to provide access to this significant new source of chemical diversity with novel/rare actinomycetes including new species of previously reported actinomycetes. Copyright © 2012 Elsevier GmbH. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                07 October 2016
                2016
                : 7
                : 1594
                Affiliations
                [1] 1Laboratorio de Productos Naturales Marinos, Facultad de Química, Universidad Nacional Autónoma de México, Unidad Sisal Sisal, Mexico
                [2] 2LAQV-REQUIMTE, Department of Chemistry, Faculty of Science and Technology, Universidade NOVA de Lisboa Caparica, Portugal
                [3] 3UCIBIO-REQUIMTE, Department of Life Sciences, Faculty of Science and Technology, Universidade NOVA de Lisboa Caparica, Portugal
                [4] 4Research Institute for Medicines (iMed.ULisboa), Faculty of Pharmacy, Universidade de Lisboa Lisbon, Portugal
                [5] 5Department of Biochemistry and Human Biology, Faculty of Pharmacy, Universidade de Lisboa Lisbon, Portugal
                Author notes

                Edited by: Alison Buchan, University of Tennessee, USA

                Reviewed by: Zongze Shao, State Oceanic Administration, China; Sarah Lydia Lebeis, University of Tennessee, USA

                *Correspondence: Susana P. Gaudêncio s.gaudencio@ 123456fct.unl.pt

                This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.01594
                5053986
                27774089
                4515df8a-0ad1-4d91-8bf5-72538f9e90ff
                Copyright © 2016 Prieto-Davó, Dias, Gomes, Rodrigues, Parera-Valadez, Borralho, Pereira, Rodrigues, Santos-Sanches and Gaudêncio.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 02 August 2016
                : 23 September 2016
                Page count
                Figures: 5, Tables: 4, Equations: 0, References: 49, Pages: 12, Words: 7918
                Funding
                Funded by: Fundação para a Ciência e a Tecnologia 10.13039/501100001871
                Award ID: PTDC/QUI-QUI/119116/2010
                Award ID: IF/00700/2014
                Award ID: UID/QUI/50006/2013
                Award ID: UID/Multi/04378/2013
                Funded by: Seventh Framework Programme 10.13039/501100004963
                Award ID: PCOFUND-GA-2009-246542
                Award ID: 269138-NanoGuard
                Funded by: Consejo Nacional de Ciencia y Tecnología 10.13039/501100007350
                Award ID: 560614
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                marine actinomycetes,marine sediments,natural product discovery,madeira archipelago,anticancer activity,antimicrobial activity,marine actinomycete phylogeny,cultivable bacterial diversity

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