An official website of the United States government
Abstract Commensal bacteria associated with marine invertebrates are underappreciated sources of chemically novel natural products. Using mass spectrometry, we had previously detected the presence of peptidic natural products in obligate marine bacteria of the genusMicrobulbifercultured from marine sponges. In this report, the isolation and structural characterization of a panel of ureidohexapeptide natural products, termed the bulbiferamides, fromMicrobulbiferstrains is reported wherein the tryptophan side chain indole participates in a macrocyclizing peptide bond formation. Genome sequencing identifies biosynthetic gene clusters encoding production of the bulbiferamides and implicates the involvement of a thioesterase in the indolic macrocycle formation. The structural diversity and widespread presence of bulbiferamides in commensal microbiomes of marine invertebrates point toward a possible ecological role for these natural products.
more »
« less
Polymer degrading marine Microbulbifer bacteria: an un(der)utilized source of chemical and biocatalytic novelty
Microbulbiferis a genus of halophilic bacteria that are commonly detected in the commensal marine microbiomes. These bacteria have been recognized for their ability to degrade polysaccharides and other polymeric materials. Increasingly,Microbulbifergenomes indicate these bacteria to be an untapped reservoir for novel natural product discovery and biosynthetic novelty. In this review, we summarize the distribution ofMicrobulbiferbacteria, activities of the various polymer degrading enzymes that these bacteria produce, and an up-to-date summary of the natural products that have been isolated fromMicrobulbiferstrains. We argue that these bacteria have been hiding in plain sight, and contemporary efforts into their genome and metabolome mining are going to lead to a proliferation ofMicrobulbifer-derived natural products in the future. We also describe, where possible, the ecological interactions of these bacteria in marine microbiomes.
more »
« less
- Award ID(s):
- 2238650
- PAR ID:
- 10614609
- Publisher / Repository:
- Beilstein J. Org. Chem.
- Date Published:
- Journal Name:
- Beilstein Journal of Organic Chemistry
- Volume:
- 20
- ISSN:
- 1860-5397
- Page Range / eLocation ID:
- 1635 to 1651
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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.more » « less
-
Traxler, Matthew F. (Ed.)ABSTRACT Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate sponges. In this study, using sponge specimens collected from Guam, the Solomon Islands, the Florida Keys, and Puerto Rico, we queried whether the presence of bromotyrosine alkaloids potentiates metabolomic and microbiome conservation among geographically distant and phylogenetically different marine sponges. A multi-omic characterization of sponge holobionts revealed vastly different metabolomic and microbiome architectures among different bromotyrosine alkaloid-harboring sponges. However, we find statistically significant correlations between the microbiomes and metabolomes, signifying that the microbiome plays an important role in shaping the overall metabolome, even in low-microbial-abundance sponges. Molecules mined from the polar metabolomes of these sponges revealed conservation of biosynthetic logic between bromotyrosine alkaloids and brominated pyrrole-imidazole alkaloids, another class of marine sponge-derived natural products. In light of prior findings postulating the sponge host itself to be the biosynthetic source of bromotyrosine alkaloids, our data now set the stage for investigating the causal relationships that dictate the microbiome-metabolome interconnectedness for marine sponges in which the microbiome may not contribute to natural product biogenesis. IMPORTANCE Our work demonstrates that phylogenetically and geographically distant sponges with very different microbiomes can harbor natural product chemical classes that are united in their core chemical structures and biosynthetic logic. Furthermore, we show that independent of geographical dispersion, natural product chemistry, and microbial abundance, overall sponge metabolomes tightly correlate with their microbiomes.more » « less
-
Biddle, Jennifer F. (Ed.)ABSTRACT Global climate change impacts marine ecosystems through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, less is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their tolerance to hypoxia. We conductedin situoxygen manipulations on a coral reef in Bahía Almirante on the Caribbean coast of Panama, which has previously experienced documented episodes of hypoxia. Naïve coral colonies (previously unexposed to hypoxia) ofSiderastrea sidereaandAgaricia lamarckiwere transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress or may represent opportunists exploiting host stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. IMPORTANCEMarine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels aroundSiderastrea sidereaandAgaricia lamarckicoloniesin situto observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress.more » « less
-
Abstract Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3762/bjoc.20.146
