Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
PLoS One
2018 Jan 01;135:e0196178. doi: 10.1371/journal.pone.0196178.
Show Gene links
Show Anatomy links
Diversity and antimicrobial potential in sea anemone and holothurian microbiomes.
León-Palmero E
,
Joglar V
,
Álvarez PA
,
Martín-Platero A
,
Llamas I
,
Reche I
.
Abstract
Marine invertebrates, as holobionts, contain symbiotic bacteria that coevolve and develop antimicrobial substances. These symbiotic bacteria are an underexplored source of new bioactive molecules to face the emerging antibiotic resistance in pathogens. Here, we explored the antimicrobial activity of bacteria retrieved from the microbiota of two sea anemones (Anemonia sulcata, Actinia equina) and two holothurians (Holothuria tubulosa, Holothuria forskali). We tested the antimicrobial activity of the isolated bacteria against pathogens with interest for human health, agriculture and aquaculture. We isolated 27 strains with antibacterial activity and 12 of these isolates also showed antifungal activity. We taxonomically identified these strains being Bacillus and Vibrio species the most representative producers of antimicrobial substances. Microbiome species composition of the two sea anemones was similar between them but differed substantially of seawater bacteria. In contrast, microbiome species composition of the two holothurian species was different between them and in comparison with the bacteria in holothurian feces and seawater. In all the holobiont microbiomes Bacteroidetes was the predominant phylum. For each microbiome, we determined diversity and the rank-abundance dominance using five fitted models (null, pre-emption, log-Normal, Zipf and Zipf-Mandelbrot). The models with less evenness (i.e. Zipf and Zipf-Mandelblot) showed the best fits in all the microbiomes. Finally, we tracked (using the V4 hypervariable region of 16S rRNA gene) the relative abundance of these 27 isolates with antibacterial activity in the total pool of sequences obtained for the microbiome of each holobiont. Coincidences, although with extremely low frequencies, were detected only in the microbiome of H. forskali. This fact suggests that these isolated bacteria belong to the long tail of rare symbiotic bacteria. Therefore, more and more sophisticated culture techniques are necessary to explore this apparently vast pool of rare symbiontic bacteria and to determine their biotechnological potentiality.
Fig 1. Relative contribution of the first ten operational taxonomical units (OTUs) in the microbiome of sea anemones and in the seawater of the aquaculture tank.OTUs relative contribution in the microbiome of (A) Anemonia sulcata, (B) Actinia equina, and (C) seawater in the tank. OTU taxon assignments are shown in S3 Table. Note “other OTUs” contribution includes different taxa for each specific holobiont and seawater.
Fig 2. Relative contribution of the first ten operational taxonomical units (OTUs) in the microbiome of holothurians, in feces and in the seawater of the aquaculture tank.OTUs relative contribution in the microbiome of (A) Holothuria forskali, (B) Holothuria tubulosa, (C) holothurian feces, and (D) seawater in the tank. OTU taxon assignments are shown in S3 Table. Note “other OTUs” contribution includes different taxa for specific each holobionts and seawater.
Fig 3. Rank Abundance Dominance (RAD) plots of the sea anemone microbiomes and seawater and the model with the best fit.RAD plots of the microbiome of (A) Anemonia sulcata, (B) Actinia equina, and (C) seawater of the tank.
Fig 4. Rank Abundance Dominance (RAD) plots of the holothurians, feces and seawater and the model with the best fit.RAD plots of the microbiome of (A) Holothuria forskali, (B) Holothuria tubulosa, (C) holothurian feces, and (D) seawater of the tank.
Afgan,
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update.
2016, Pubmed
Afgan,
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update.
2016,
Pubmed
Barbosa,
Class I and Class II Lanthipeptides Produced by Bacillus spp.
2015,
Pubmed
Beauregard,
The detection and isolation of a novel antimicrobial peptide from the echinoderm, Cucumaria frondosa.
2001,
Pubmed
,
Echinobase
Bhatnagar,
Immense essence of excellence: marine microbial bioactive compounds.
2010,
Pubmed
Blunt,
Marine natural products.
2015,
Pubmed
Bordenstein,
Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.
2015,
Pubmed
Bostock,
Aquaculture: global status and trends.
2010,
Pubmed
Braña,
Two Streptomyces species producing antibiotic, antitumor, and anti-inflammatory compounds are widespread among intertidal macroalgae and deep-sea coral reef invertebrates from the central Cantabrian Sea.
2015,
Pubmed
,
Echinobase
Brosius,
Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli.
1978,
Pubmed
Cabello,
Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment.
2006,
Pubmed
Caporaso,
PyNAST: a flexible tool for aligning sequences to a template alignment.
2010,
Pubmed
Caporaso,
QIIME allows analysis of high-throughput community sequencing data.
2010,
Pubmed
Careaga,
Patagonicosides B and C, two antifungal sulfated triterpene glycosides from the sea cucumber Psolus patagonicus.
2011,
Pubmed
,
Echinobase
Chaston,
Common trends in mutualism revealed by model associations between invertebrates and bacteria.
2010,
Pubmed
Chludil,
Cytotoxic and antifungal triterpene glycosides from the Patagonian sea cucumber Hemoiedema spectabilis.
2002,
Pubmed
,
Echinobase
DeSantis,
Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.
2006,
Pubmed
Defoirdt,
Alternatives to antibiotics for the control of bacterial disease in aquaculture.
2011,
Pubmed
Donia,
Marine natural products and their potential applications as anti-infective agents.
2003,
Pubmed
Edgar,
Search and clustering orders of magnitude faster than BLAST.
2010,
Pubmed
ElAhwany,
Phylogenetic diversity and antimicrobial activity of marine bacteria associated with the soft coral Sarcophyton glaucum.
2015,
Pubmed
Enomoto,
Microbial communities associated with holothurians: presence of unique bacteria in the coelomic fluid.
2012,
Pubmed
,
Echinobase
Fenical,
Developing a new resource for drug discovery: marine actinomycete bacteria.
2006,
Pubmed
Galand,
Ecology of the rare microbial biosphere of the Arctic Ocean.
2009,
Pubmed
Gao,
Antibacterial and antilarval compounds from marine gorgonian-associated bacterium Bacillus amyloliquefaciens SCSIO 00856.
2010,
Pubmed
Gao,
Bacterial community composition in the gut content and ambient sediment of sea cucumber Apostichopus japonicus revealed by 16S rRNA gene pyrosequencing.
2014,
Pubmed
,
Echinobase
Gowda,
T-antigen binding lectin with antibacterial activity from marine invertebrate, sea cucumber (Holothuria scabra): possible involvement in differential recognition of bacteria.
2008,
Pubmed
,
Echinobase
Haug,
Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea).
2002,
Pubmed
,
Echinobase
Kang,
Marine peptides and their anti-infective activities.
2015,
Pubmed
Kearse,
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.
2012,
Pubmed
Kumar,
Antifungal activity in triterpene glycosides from the sea cucumber Actinopyga lecanora.
2007,
Pubmed
,
Echinobase
Le Roux,
The emergence of Vibrio pathogens in Europe: ecology, evolution, and pathogenesis (Paris, 11-12th March 2015).
2015,
Pubmed
Ling,
A new antibiotic kills pathogens without detectable resistance.
2015,
Pubmed
Lok,
Mining the microbial dark matter.
2015,
Pubmed
Martens,
Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont.
2009,
Pubmed
Martín-Platero,
Fast, convenient, and economical method for isolating genomic DNA from lactic acid bacteria using a modification of the protein "salting-out" procedure.
2007,
Pubmed
Maynard,
Reciprocal interactions of the intestinal microbiota and immune system.
2012,
Pubmed
McFall-Ngai,
Host-microbe symbiosis: the squid-Vibrio association--a naturally occurring, experimental model of animal/bacterial partnerships.
2008,
Pubmed
Meron,
Changes in microbial communities associated with the sea anemone Anemonia viridis in a natural pH gradient.
2013,
Pubmed
Miller,
A simple salting out procedure for extracting DNA from human nucleated cells.
1988,
Pubmed
Molinski,
Drug development from marine natural products.
2009,
Pubmed
Montesinos,
Development, registration and commercialization of microbial pesticides for plant protection.
2003,
Pubmed
Moore,
Biosynthesis of marine natural products: microorganisms and macroalgae.
1999,
Pubmed
Natrah,
Disruption of bacterial cell-to-cell communication by marine organisms and its relevance to aquaculture.
2011,
Pubmed
Omran,
Screening of microbial contamination and antimicrobial activity of sea cucumber Holothuria polii.
2013,
Pubmed
,
Echinobase
Paul,
Marine chemical ecology in benthic environments.
2011,
Pubmed
Pedrós-Alió,
The rare bacterial biosphere.
2012,
Pubmed
Pedrós-Alió,
Marine microbial diversity: can it be determined?
2006,
Pubmed
Piel,
Metabolites from symbiotic bacteria.
2009,
Pubmed
Rinke,
Insights into the phylogeny and coding potential of microbial dark matter.
2013,
Pubmed
Rosenberg,
The role of microorganisms in coral health, disease and evolution.
2007,
Pubmed
Saiki,
Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.
1988,
Pubmed
Sansinenea,
Secondary metabolites of soil Bacillus spp.
2011,
Pubmed
Schloss,
Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.
2009,
Pubmed
Schmitt,
Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges.
2012,
Pubmed
Silchenko,
Holothurins B(2), B(3), and B(4), new triterpene glycosides from mediterranean sea cucumbers of the genus holothuria.
2005,
Pubmed
,
Echinobase
Sogin,
Microbial diversity in the deep sea and the underexplored "rare biosphere".
2006,
Pubmed
Sun,
Pyrosequencing reveals diverse microbial community associated with the zoanthid Palythoa australiae from the South China Sea.
2014,
Pubmed
Tagg,
Assay system for bacteriocins.
1971,
Pubmed
Tareq,
Gageopeptins A and B, new inhibitors of zoospore motility of the phytopathogen Phytophthora capsici from a marine-derived bacterium Bacillus sp. 109GGC020.
2015,
Pubmed
Theis,
Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes.
2016,
Pubmed
Valliappan,
Marine actinobacteria associated with marine organisms and their potentials in producing pharmaceutical natural products.
2014,
Pubmed
Wang,
Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.
2007,
Pubmed
Webster,
Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts.
2010,
Pubmed
Whittaker,
Dominance and Diversity in Land Plant Communities: Numerical relations of species express the importance of competition in community function and evolution.
1965,
Pubmed
Wijffels,
Potential of sponges and microalgae for marine biotechnology.
2008,
Pubmed
Zhang,
Phylogenetic survey and antimicrobial activity of culturable microorganisms associated with the South China Sea black coral Antipathes dichotoma.
2012,
Pubmed
Zhang,
Bioactive triterpene glycosides from the sea cucumber Holothuria fuscocinerea.
2006,
Pubmed
,
Echinobase
