Abstract
Historically, marine invertebrates have been a prolific source of unique natural products, with a diverse array of biological activities. Recent studies of invertebrate-associated microbial communities are revealing microorganisms as the true producers of many of these compounds. Inspired by the human microbiome project, which has highlighted the human intestine as a unique microenvironment in terms of microbial diversity, we elected to examine the bacterial communities of fish intestines (which we have termed the fish microbiome) as a new source of microbial and biosynthetic diversity for natural products discovery. To test the hypothesis that the fish microbiome contains microorganisms with unique capacity for biosynthesizing natural products, we examined six species of fish through a combination of dissection and culture-dependent evaluation of intestinal microbial communities. Using isolation media designed to enrich for marine Actinobacteria, we have found three main clades that show taxonomic divergence from known strains, several of which are previously uncultured. Extracts from these strains exhibit a wide range of activities against both Gram-positive and Gram-negative human pathogens, as well as several fish pathogens. Exploration of one of these extracts has identified the novel bioactive lipid sebastenoic acid as an anti-microbial agent, with activity against Staphylococcus aureus, Bacillus subtilis, Enterococcus faecium, and Vibrio mimicus.
Highlights
Marine invertebrates have been a mainstay for the discovery of novel natural products scaffolds
[1] More recently, attention has focused on the symbiotic and mutualistic microbial communities living within these sessile marine organisms. Careful examination of these communities using a variety of microbiological and molecular techniques is revealing that microorganisms are the true producers of many of the compounds first isolated from host invertebrates. [2,3] Terrestrial microorganisms, especially those from the order Actinomycetales, formed the backbone for the golden age of antibiotic discovery, and are the source of the vast majority of FDA-approved antimicrobial agents
[6] Emphasis on these unexplored microenvironments has garnered significant attention among the natural product community over the last few years. Examples of these unique environments include hydrothermal vents and invertebrate hosts, such as nematodes. [7,8,9,10] Along these same lines, researchers have examined Actinobacteria from dissected mud daber wasps, and uncovered 15 diverse strains of Streptomyces spp., one of which led to the isolation of a novel antifungal macrocyclic lactam. [11,12] Separately, a different research program connected with the Philippine International Cooperative for Biodiversity Groups (ICBG) program has successfully isolated novel bioactive natural products from mollusks and cone snails by culturing symbiotic bacteria from the tissues of these gastropods. [13,14,15]
Summary
Marine invertebrates have been a mainstay for the discovery of novel natural products scaffolds. We present the first report of the examination of the fish microbiome as a source of microbial diversity for natural products research. This study has resulted in the isolation of taxonomically distinct Actinomycetales from fish intestines, as well as unique strains of Firmicutes and Proteobacteria.
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