scholarly journals Isolation and genome sequencing of 14 Spongia sp. bacterial associates expands the taxonomic and functional breadth of the cultivatable marine sponge microbiome

2020 ◽  
Author(s):  
Elham Karimi ◽  
Rodrigo Costa

AbstractMarine sponges live with complex microbial consortia, which have been considered as potential sources of novel natural products. However, the usual recalcitrance of host-associated microorganisms to cultivation makes studying sponge symbionts challenging. To tackle this complexity, exploration of cultivated sponge-associated bacteria and their coding potential is unavoidable. In this study, we isolate and report the draft genome sequences of 14 bacterial strains from the marine sponge Spongia sp. using R2A and VXA media. The strains belong to the classes Actinobacteria, Gammaproteobacteria, Alphaproteobacteria, and Cytophagia spanning 11 formally described genera plus two potentially novel genera in the Rhodobacteraceae family and one potentially novel family in the Cytophagales order. Functional genomics revealed presumed symbiosis factors typical of specific taxonomic groups (i.e. taurine metabolism genes among the Alphaproteobacteria, chitinase encoding genes and eukaryotic-like proteins in the Cytophagia genome) while multidrug efflux pumps, also important in host-microbe interactions, were common across all genomes. Moreover, we detected 76 secondary-metabolite biosynthetic gene clusters putatively involved in the production of drug-like compounds or signalling molecules across all genomes, warranting future biotechnologically driven research into their coding potential.

2019 ◽  
Vol 7 (12) ◽  
pp. 635
Author(s):  
Anoop Alex ◽  
Agostinho Antunes

The most recently described bacterial members of the genus Endozoicomonas have been found in association with a wide variety of marine invertebrates. Despite their ubiquity in the host holobiont, limited information is available on the molecular genomic signatures of the symbiotic association of Endozoicomonas with marine sponges. Here, we generated a draft genome of Endozoicomonas sp. OPT23 isolated from the intertidal marine sponge Ophlitaspongia papilla and performed comprehensive comparative genomics analyses. Genome-specific analysis and metabolic pathway comparison of the members of the genus Endozoicomonas revealed the presence of gene clusters encoding for unique metabolic features, such as the utilization of carbon sources through lactate, L-rhamnose metabolism, and a phenylacetic acid degradation pathway in Endozoicomonas sp. OPT23. Moreover, the genome harbors genes encoding for eukaryotic-like proteins, such as ankyrin repeats, tetratricopeptide repeats, and Sel1 repeats, which likely facilitate sponge-bacterium attachment. The genome also encodes major secretion systems and homologs of effector molecules that seem to enable the sponge-associated bacterium to interact with the sponge and deliver the virulence factors for successful colonization. In conclusion, the genome analysis of Endozoicomonas sp. OPT23 revealed the presence of adaptive genomic signatures that might favor their symbiotic lifestyle within the sponge host.


2020 ◽  
Author(s):  
Mathew Storey ◽  
SK Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert Keyzers ◽  
...  

© 2020 Storey et al. Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metag-enomic investigation of Mycale hentscheli, a chemically gifted marine sponge that pos-sesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short-and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemo-types. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holo-biont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These re-sults suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small mol-ecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing mi-crobe. We also find that the microbiome of M. hentscheli is stably maintained among in-dividuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.


Marine Drugs ◽  
2020 ◽  
Vol 18 (2) ◽  
pp. 124 ◽  
Author(s):  
Ipsita Mohanty ◽  
Sheila Podell ◽  
Jason S. Biggs ◽  
Neha Garg ◽  
Eric E. Allen ◽  
...  

Marine sponge holobionts, defined as filter-feeding sponge hosts together with their associated microbiomes, are prolific sources of natural products. The inventory of natural products that have been isolated from marine sponges is extensive. Here, using untargeted mass spectrometry, we demonstrate that sponges harbor a far greater diversity of low-abundance natural products that have evaded discovery. While these low-abundance natural products may not be feasible to isolate, insights into their chemical structures can be gleaned by careful curation of mass fragmentation spectra. Sponges are also some of the most complex, multi-organismal holobiont communities in the oceans. We overlay sponge metabolomes with their microbiome structures and detailed metagenomic characterization to discover candidate gene clusters that encode production of sponge-derived natural products. The multi-omic profiling strategy for sponges that we describe here enables quantitative comparison of sponge metabolomes and microbiomes to address, among other questions, the ecological relevance of sponge natural products and for the phylochemical assignment of previously undescribed sponge identities.


mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Mathew A. Storey ◽  
Sarah K. Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert A. Keyzers ◽  
...  

ABSTRACT Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metagenomic investigation of Mycale hentscheli, a chemically gifted marine sponge that possesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short- and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemotypes. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holobiont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These results suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small molecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing microbe. We also find that the microbiome of M. hentscheli is stably maintained among individuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.


2020 ◽  
Author(s):  
Mathew Storey ◽  
SK Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert Keyzers ◽  
...  

© 2020 Storey et al. Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metag-enomic investigation of Mycale hentscheli, a chemically gifted marine sponge that pos-sesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short-and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemo-types. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holo-biont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These re-sults suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small mol-ecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing mi-crobe. We also find that the microbiome of M. hentscheli is stably maintained among in-dividuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.


2020 ◽  
Vol 4 ◽  
Author(s):  
Francis E. Sakai-Kawada ◽  
Courtney G. Ip ◽  
Kehau A. Hagiwara ◽  
Hoang-Yen X. Nguyen ◽  
Christopher-James A. V. Yakym ◽  
...  

Interest in bioactive pigments stems from their ecological role in adaptation, as well as their applications in various consumer products. The production of these bioactive pigments can be from a variety of biological sources, including simple microorganisms that may or may not be associated with a host. This study is particularly interested in the marine sponges, which have been known to harbor microorganisms that produce secondary metabolites like bioactive pigments. In this study, marine sponge tissue samples were collected from Puhi Bay off the Eastern shore of Hilo, Hawai‘i and subsequently were identified as Petrosia sp. with red pigmentation. Using surface sterilization and aseptic plating of sponge tissue samples, sponge-associated microorganisms were isolated. One isolate (PPB1) produced a colony with red pigmentation like that of Petrosia sp., suggesting an integral relationship between this particular isolate and the sponge of interest. 16S characterization and sequencing of PPB1 revealed that it belonged to the Pseudoalteromonas genus. Using various biological assays, both antimicrobial and antioxidant bioactivity was shown in Pseudoalteromonas sp. PPB1 crude extract. To further investigate the genetics of pigment production, a draft genome of PPB1 was sequenced, assembled, and annotated. This revealed a prodiginine biosynthetic pathway and the first cited-incidence of a prodiginine-producing Pseudoalteromonas species isolated from a marine sponge host. Further understanding into the bioactivity and biosynthesis of secondary metabolites like pigmented prodiginine may uncover the complex ecological interactions between host sponge and microorganism.


2020 ◽  
Vol 9 (31) ◽  
Author(s):  
M. Alejandro Dinamarca ◽  
Karoll González-Pizarro ◽  
Rebeca Ahumada ◽  
Claudia Ibacache-Quiroga

ABSTRACT Kefir is an ancestral food produced using microbial consortia whose composition varies depending on the geographical origin and the substrate used for fermentation. This dairy beverage is considered a probiotic food, and its consumption has been associated with several health benefits. This report describes the isolation of bacterial strains from Chilean kefir.


2019 ◽  
Vol 09 ◽  
Author(s):  
Rahanira Ralambondrahety ◽  
Aurélie Couzinet-Mossion ◽  
Vony Rabesaotra ◽  
Onja Andriambeloson ◽  
Gilles Barnathan ◽  
...  

Background: Nowadays, the efficiency of antibiotics is endangered by the development of resistant bacterial strains. Consequently, novel bioactive agents are intensively searched. Marine sponges are well-known for being major sources of bioactive compounds, including unusual sterols. Until now, among sterols, interesting antibacterial activity has been reported exclusively for Δ5 sterols. Objectives: This study aims to describe the steroid composition of the marine sponge Biemna laboutei collected in the North coast of Madagascar, and the antibacterial activity of steroid mixture against human pathogenic strains. Methods: Sponge was extracted in CHCl3/MeOH. Free steroids were separated from other lipids by column chromatography with dichloromethane as specific eluent. Free sterols/steroids and sterol acetates were analyzed by gas chromatography coupled with mass spectrometry. Antibacterial activity (Minimum inhibitory concentration, MIC) of steroid fractions was assessed for eight strains using agar diffusion with cellulose disks. Results: Neutral lipids were the major lipid class (79.1% of total lipids) and the dichloromethane eluted fraction contained only free steroids giving rise to the identification of eleven compounds. These components presented exclusively Δ7 unsaturation, including lathosterol as major one (38.4%) and four 3-oxo-steroids (11.8%). The steroid fraction of B. laboutei has demonstrated efficiency against pathogenic strains but more specifically on the gram(+) Bacillus cereus (MIC of 12.5 µg/mL) and Staphylococcus aureus (MIC of 25 µg/mL). This latter bacterium causes several illnesses, some of those strains being antibiotic-resistant and this becomes a worldwide health problem. Conclusion: This is the first report for an antibacterial activity of a mixture of Δ7 steroids against a resistant strain of S. aureus to many antibiotics.


2019 ◽  
Vol 12 (1) ◽  
pp. 3647-3655 ◽  
Author(s):  
Elham Karimi ◽  
Enora Geslain ◽  
Hetty KleinJan ◽  
Gwenn Tanguy ◽  
Erwan Legeay ◽  
...  

Abstract Brown algae are important primary producers and ecosystem engineers in the ocean, and Ectocarpus has been established as a laboratory model for this lineage. Like most multicellular organisms, Ectocarpus is associated with a community of microorganisms, a partnership frequently referred to as holobiont due to the tight interconnections between the components. Although genomic resources for the algal host are well established, its associated microbiome is poorly characterized from a genomic point of view, limiting the possibilities of using these types of data to study host–microbe interactions. To address this gap in knowledge, we present the annotated draft genome sequences of seventy-two cultivable Ectocarpus-associated bacteria. A screening of gene clusters related to the production of secondary metabolites revealed terpene, bacteriocin, NRPS, PKS-t3, siderophore, PKS-t1, and homoserine lactone clusters to be abundant among the sequenced genomes. These compounds may be used by the bacteria to communicate with the host and other microbes. Moreover, detoxification and provision of vitamin B pathways have been observed in most sequenced genomes, highlighting potential contributions of the bacterial metabolism toward host fitness and survival. The genomes sequenced in this study form a valuable resource for comparative genomic analyses and evolutionary surveys of alga-associated bacteria. They help establish Ectocarpus as a model for brown algal holobionts and will enable the research community to produce testable hypotheses about the molecular interactions within this complex system.


2015 ◽  
Vol 3 (5) ◽  
Author(s):  
Hannes Horn ◽  
Ute Hentschel ◽  
Usama Ramadan Abdelmohsen

Here, we report the draft genome sequences of three actinobacterial isolates, Micromonospora sp. RV43, Rubrobacter sp. RV113, and Nocardiopsis sp. RV163 that had previously been isolated from Mediterranean sponges. The draft genomes were analyzed for the presence of gene clusters indicative of secondary metabolism using antiSMASH 3.0 and NapDos pipelines. Our findings demonstrated the chemical richness of sponge-associated actinomycetes and the efficacy of genome mining in exploring the genomic potential of sponge-derived actinomycetes.


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