scholarly journals Metagenomic exploration of the marine sponge mycale hentscheli uncovers multiple polyketide-producing bacterial symbionts

2020 ◽  
Author(s):  
Mathew Storey ◽  
SK Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert Keyzers ◽  
...  
Keyword(s):  
Marine Sponge ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Taxonomic Diversity ◽  
Marine Sponges ◽  
Metagenomic Sequencing ◽  
Defensive Symbiosis ◽  
Long Read ◽  
Comprehensive Picture ◽  
Mycale Hentscheli

© 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.

scholarly journals Metagenomic exploration of the marine sponge mycale hentscheli uncovers multiple polyketide-producing bacterial symbionts

2020 ◽  
Author(s):  
Mathew Storey ◽  
SK Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert Keyzers ◽  
...  
Keyword(s):  
Marine Sponge ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Taxonomic Diversity ◽  
Marine Sponges ◽  
Metagenomic Sequencing ◽  
Defensive Symbiosis ◽  
Long Read ◽  
Comprehensive Picture ◽  
Mycale Hentscheli

© 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.

scholarly journals Metagenomic Exploration of the Marine Sponge Mycale hentscheli Uncovers Multiple Polyketide-Producing Bacterial Symbionts

mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Mathew A. Storey ◽  
Sarah K. Andreassend ◽  
Joe Bracegirdle ◽  
Alistair Brown ◽  
Robert A. Keyzers ◽  
...  
Keyword(s):  
Marine Sponge ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Taxonomic Diversity ◽  
Marine Sponges ◽  
Metagenomic Sequencing ◽  
Content Type ◽  
Defensive Symbiosis ◽  
Long Read ◽  
Mycale Hentscheli

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.

scholarly journals Biosynthetic potential of uncultured Antarctic soil bacteria revealed through long-read metagenomic sequencing

2021 ◽  
Author(s):  
Valentin Waschulin ◽  
Chiara Borsetto ◽  
Robert James ◽  
Kevin K. Newsham ◽  
Stefano Donadio ◽  
...  
Keyword(s):  
Genome Mining ◽  
Gene Clusters ◽  
Biosynthetic Gene Cluster ◽  
Full Length ◽  
Metagenomic Sequencing ◽  
Short Read ◽  
Short Read Sequencing ◽  
Rich Diversity ◽  
Long Read ◽  
The Rich

AbstractThe growing problem of antibiotic resistance has led to the exploration of uncultured bacteria as potential sources of new antimicrobials. PCR amplicon analyses and short-read sequencing studies of samples from different environments have reported evidence of high biosynthetic gene cluster (BGC) diversity in metagenomes, indicating their potential for producing novel and useful compounds. However, recovering full-length BGC sequences from uncultivated bacteria remains a challenge due to the technological restraints of short-read sequencing, thus making assessment of BGC diversity difficult. Here, long-read sequencing and genome mining were used to recover >1400 mostly full-length BGCs that demonstrate the rich diversity of BGCs from uncultivated lineages present in soil from Mars Oasis, Antarctica. A large number of highly divergent BGCs were not only found in the phyla Acidobacteriota, Verrucomicrobiota and Gemmatimonadota but also in the actinobacterial classes Acidimicrobiia and Thermoleophilia and the gammaproteobacterial order UBA7966. The latter furthermore contained a potential novel family of RiPPs. Our findings underline the biosynthetic potential of underexplored phyla as well as unexplored lineages within seemingly well-studied producer phyla. They also showcase long-read metagenomic sequencing as a promising way to access the untapped genetic reservoir of specialised metabolite gene clusters of the uncultured majority of microbes.

scholarly journals Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type

2019 ◽  
Author(s):  
Allison M. Sharrar ◽  
Alexander Crits-Christoph ◽  
Raphaël Méheust ◽  
Spencer Diamond ◽  
Evan P. Starr ◽  
...  
Keyword(s):  
Secondary Metabolite ◽  
Vegetation Type ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Metagenomic Sequencing ◽  
Soil Bacterial Diversity ◽  
Community Members ◽  
Clinical Value ◽  
Specialized Metabolites ◽  
Shallow Soils

AbstractBacteria isolated from soils are major sources of specialized metabolites, including antibiotics and other compounds with clinical value that likely shape interactions among microbial community members and impact biogeochemical cycles. Yet, isolated lineages represent a small fraction of all soil bacterial diversity. It remains unclear how the production of specialized metabolites varies across the phylogenetic diversity of bacterial species in soils, and whether the genetic potential for production of these metabolites differs with soil type. We sampled soils and saprolite from three sites in a northern California Critical Zone Observatory with varying vegetation and bedrock characteristics and used metagenomic sequencing and assembly to reconstruct 1,334 microbial genomes containing diverse biosynthetic gene clusters (BGCs) for secondary metabolite production. We obtained genomes for prolific producers of secondary metabolites, including novel groups within the Actinobacteria, Chloroflexi and candidate phylum Dormibactereota. Surprisingly, one genome of a Candidate Phyla Radiation bacterium encoded for a ribosomally synthesized linear azole/azoline-containing peptide, a capacity we found in other publicly available CPR bacterial genomes. Overall, bacteria with higher biosynthetic potential were enriched in shallow soils and grassland soils, with patterns of abundance of BGC type varying by taxonomy.

scholarly journals Multi-Omic Profiling of Melophlus Sponges Reveals Diverse Metabolomic and Microbiome Architectures that Are Non-overlapping with Ecological Neighbors

Marine Drugs ◽  
2020 ◽  
Vol 18 (2) ◽  
pp. 124 ◽  
Author(s):  
Ipsita Mohanty ◽  
Sheila Podell ◽  
Jason S. Biggs ◽  
Neha Garg ◽  
Eric E. Allen ◽  
...  
Keyword(s):  
Mass Spectrometry ◽  
Natural Products ◽  
Candidate Gene ◽  
Marine Sponge ◽  
Gene Clusters ◽  
Marine Sponges ◽  
Quantitative Comparison ◽  
Filter Feeding ◽  
Chemical Structures ◽  
Ecological Relevance

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.

scholarly journals Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics

2021 ◽  
Author(s):  
Marc W. Van Goethem ◽  
Andrew R. Osborn ◽  
Benjamin P. Bowen ◽  
Peter F. Andeer ◽  
Tami L. Swenson ◽  
...  
Keyword(s):  
Secondary Metabolites ◽  
Temporal Dynamics ◽  
Functional Characterization ◽  
Gene Clusters ◽  
Metagenomic Sequencing ◽  
Pronounced Increase ◽  
Environmental Processes ◽  
Soil Communities ◽  
Functional Dynamics ◽  
Long Read

AbstractMicrobial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and assembly of metagenomes from biological soil crusts, a group of soil communities that are rich in BGCs. Taking advantage of the unusually long assemblies produced by this approach, we recovered nearly 3,000 BGCs for analysis, including 695 novel, full-length BGCs. Functional exploration through metatranscriptome analysis of a 3-day wetting experiment uncovered phylum-specific BGC expression upon activation from dormancy, elucidating distinct roles and complex phylogenetic and temporal dynamics in wetting processes. For example, a pronounced increase in BGC transcription occurs at night in cyanobacteria but not in other phyla, implicating BGCs in nutrient scavenging roles and niche competition. Taken together, our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts.

scholarly journals Comparative Genomics Reveals Metabolic Specificity of Endozoicomonas Isolated from a Marine Sponge and the Genomic Repertoire for Host-Bacteria Symbioses

2019 ◽  
Vol 7 (12) ◽  
pp. 635
Author(s):  
Anoop Alex ◽  
Agostinho Antunes
Keyword(s):  
Comparative Genomics ◽  
Marine Sponge ◽  
Draft Genome ◽  
Carbon Sources ◽  
Gene Clusters ◽  
Marine Sponges ◽  
Symbiotic Association ◽  
Limited Information ◽  
Secretion Systems ◽  
Genomic Signatures

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.

scholarly journals Metagenomic Insights Into the Microbial Communities of Inert and Oligotrophic Outdoor Pier Surfaces of a Coastal City

2021 ◽  
Author(s):  
Xinzhao Tong ◽  
Marcus H. Y. Leung ◽  
Zhiyong Shen ◽  
Justin Y. Y. Lee ◽  
Christopher E. Mason ◽  
...  
Keyword(s):  
Microbial Communities ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Taxonomic Composition ◽  
Metagenomic Sequencing ◽  
Biosynthetic Gene Clusters ◽  
Metabolic Functions ◽  
Outdoor Spaces ◽  
Genomic Characterization ◽  
Indoor Spaces

Abstract Background: Studies of the microbiomes on surfaces in built environment have largely focused on indoor spaces, while outdoor spaces have received far less attention. Piers are engineered infrastructures commonly found in coastal areas, and due to their unique locations at the interface between terrestrial and aquatic ecosystems, pier surfaces are likely to harbor interesting microbiology. In this study, the microbiomes on the metal and concrete surfaces at nine piers located along the coastline of Hong Kong were investigated by metagenomic sequencing. The roles played by different factors in shaping the taxonomic composition and functional traits of the pier surface microbiomes were determined. Metagenome-assembled genomes were reconstructed and their putative biosynthetic gene clusters were characterized in detail.Results: Surface material was found to be the strongest factor in structuring the taxonomic and functional compositions of the pier surface microbiomes. Corrosion-related bacteria were significantly enriched on metal surfaces, consistent with the pitting corrosion observed. The differential enrichment of taxa mediating biodegradation suggests differences between the metal and concrete surfaces in terms of specific xenobiotics being potentially degraded. Genome-centric analysis detected the presence of many novel species, with the majority of them belonging to the phylum Proteobacteria. Genomic characterization showed that the potential metabolic functions and secondary biosynthetic capacity were largely governed by taxonomy, rather than surface attributes and geography. Conclusions: Pier surfaces are a rich reservoir of abundant novel bacterial species. Members of the surface microbial communities use different mechanisms to counter the stresses under oligotrophic conditions. A better understanding of the outdoor surface microbiomes located in different environments should enhance the ability to maintain outdoor surfaces of infrastructures.

scholarly journals Metagenomic insights into the microbial communities of inert and oligotrophic outdoor pier surfaces of a coastal city

Microbiome ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Xinzhao Tong ◽  
Marcus H. Y. Leung ◽  
Zhiyong Shen ◽  
Justin Y. Y. Lee ◽  
Christopher E. Mason ◽  
...  
Keyword(s):  
Microbial Communities ◽  
Bacterial Species ◽  
Gene Clusters ◽  
Taxonomic Composition ◽  
Metagenomic Sequencing ◽  
Metabolic Functions ◽  
Outdoor Spaces ◽  
Physical Attributes ◽  
Genomic Characterization ◽  
Indoor Spaces

Abstract Background Studies of the microbiomes on surfaces in built environment have largely focused on indoor spaces, while outdoor spaces have received far less attention. Piers are engineered infrastructures commonly found in coastal areas, and due to their unique locations at the interface between terrestrial and aquatic ecosystems, pier surfaces are likely to harbor interesting microbiology. In this study, the microbiomes on the metal and concrete surfaces at nine piers located along the coastline of Hong Kong were investigated by metagenomic sequencing. The roles played by different physical attributes and environmental factors in shaping the taxonomic composition and functional traits of the pier surface microbiomes were determined. Metagenome-assembled genomes were reconstructed and their putative biosynthetic gene clusters were characterized in detail. Results Surface material was found to be the strongest factor in structuring the taxonomic and functional compositions of the pier surface microbiomes. Corrosion-related bacteria were significantly enriched on metal surfaces, consistent with the pitting corrosion observed. The differential enrichment of taxa mediating biodegradation suggests differences between the metal and concrete surfaces in terms of specific xenobiotics being potentially degraded. Genome-centric analysis detected the presence of many novel species, with the majority of them belonging to the phylum Proteobacteria. Genomic characterization showed that the potential metabolic functions and secondary biosynthetic capacity were largely correlated with taxonomy, rather than surface attributes and geography. Conclusions Pier surfaces are a rich reservoir of abundant novel bacterial species. Members of the surface microbial communities use different mechanisms to counter the stresses under oligotrophic conditions. A better understanding of the outdoor surface microbiomes located in different environments should enhance the ability to maintain outdoor surfaces of infrastructures.

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
Keyword(s):  
Marine Sponge ◽  
Draft Genome ◽  
Gene Clusters ◽  
Marine Sponges ◽  
Microbial Consortia ◽  
Bacterial Strains ◽  
Signalling Molecules ◽  
Host Microbe Interactions ◽  
Taxonomic Groups ◽  
Coding Potential

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.

Sign in / Sign up

Export Citation Format

Share Document