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Jensen, P. R.

Publications and source records attributed to Jensen, P. R..

4 recordsLinked to original sources

Microbial diversity in tropical marine sediments assessed using culture-dependent and culture-independent techniques

The microbial communities associated with marine sediments are critical for ecosystem function yet remain poorly characterized. While culture-independent (CI) approaches capture the broadest perspective on community composition, culture-dependent (CD) methods can capture low abundance taxa that are missed using CI approaches. The aim of this study was to assess microbial diversity in tropical marine sediments collected from five shallow water sites in Belize using both CD and CI approaches. CD methods captured approximately 3% of the >800 genera detected across the five sites. Additionally, 39 genera were only detected using CD approaches revealing rare taxa that were missed with the CI approach. Significantly different communities were detected across sites, with rare taxa playing an important role in the delineation of sediment communities. This study provides important baseline data describing shallow water sediment microbial communities and evidence that standard cultivation techniques may be more effective than previously recognized. Originality-Significance StatementMarine sediments host some of the most diverse microbial communities on the planet. While these communities are critical for global nutrient cycling, the oceanic food web, and the maintenance of ecosystem dynamics, they remain poorly studied. Studies that have assessed sediment communities typically use culture-independent approaches, which have known biases and can miss ecologically important taxa. Here we describe microbial diversity in marine sediments using both culture-dependent and culture-independent approaches. Our culturing approach, sequencing communities as opposed to individual colonies, revealed an additional 39 genera that were not detected with culture-independent methods. Additionally, we cultured numerous, as-yet undescribed species, suggesting that traditional culturing practices can be more efficient than commonly thought. Moreover, our results indicate rare taxa play an important role in distinguishing microbial communities at different sites, thus highlighting the importance of deep sequencing and incorporating culture-dependent approaches for diversity assessments.

microbiology↗

Complex evolutionary dynamics govern the diversity and distribution of biosynthetic gene clusters and their encoded specialized metabolites

While specialized metabolites are thought to mediate ecological interactions, the evolutionary processes driving their diversification, particularly among closely related lineages, remain poorly understood. Here, we examine the evolutionary dynamics governing the distribution of natural product biosynthetic gene clusters (BGCs) using 118 strains within the marine actinomycete genus Salinispora. While previous evidence indicated that horizontal gene transfer (HGT) largely contributed to BGC diversity, we find that a majority of BGCs in Salinispora genomes are conserved through processes of vertical descent. In particular, vertical inheritance maintained BGCs over evolutionary timescales (millions of years) allowing for BGC diversification among Salinispora species. By coupling the genomic analyses with high-resolution tandem mass spectrometry (LC-MS/MS), we identified that BGC evolution in Salinispora proceeds largely through gene gain/loss events and constrained recombination that contributes to interspecies diversity at the gene, pathway, and metabolite levels. Consequently, the evolutionary processes driving BGC diversification had direct consequences for compound production and contributed to chemical diversification, as exemplified in our case study of the medically relevant proteosome inhibitors, the salinosporamides. Together, our results support the concept that specialized metabolites, and their cognate BGCs, represent functional traits associated with niche differentiation among Salinispora species. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=107 SRC="FIGDIR/small/423547v2_ufig1.gif" ALT="Figure 1"> View larger version (21K): org.highwire.dtl.DTLVardef@aef190org.highwire.dtl.DTLVardef@17536baorg.highwire.dtl.DTLVardef@5bf336org.highwire.dtl.DTLVardef@bc7d2f_HPS_FORMAT_FIGEXP M_FIG C_FIG O_TEXTBOXSIGNIFICANCENatural products are traditionally exploited for their pharmaceutical potential; yet what is often overlooked is that the evolution of the biosynthetic gene clusters (BGCs) encoding these small molecules likely affects the diversification of the produced compounds and implicitly has an impact on the compounds activities and ecological functions. And while the prevailing dogma in natural product research attributes frequent and widespread horizontal gene transfer (HGT) as an integral driver of BGC evolution, we find that the majority of BGC diversity derives from processes of vertical descent, with HGT events being rare. This understanding can facilitate informed biosynthetic predictions to identify novel natural products, in addition to uncovering how these specialized metabolites contribute to the environmental distribution of microbes. C_TEXTBOX

microbiology↗

Phylogenetic analysis of the salinipostin γ-butyrolactone gene cluster uncovers new potential for bacterial signaling-molecule diversity

Bacteria communicate by small-molecule chemicals that facilitate intra- and inter-species interactions. These extracellular signaling molecules mediate diverse processes including virulence, bioluminescence, biofilm formation, motility, and specialized metabolism. The signaling molecules produced by members of the phylum Actinobacteria are generally comprised of {gamma}-butyrolactones, {gamma}-butenolides, and furans. The best known actinomycete {gamma}-butyrolactone is A-factor, which triggers specialized metabolism and morphological differentiation in the genus Streptomyces. Salinipostins A-K are unique {gamma}-butyrolactone molecules with rare phosphotriester moieties that were recently characterized from the marine actinomycete genus Salinispora. The production of these compounds has been linked to the 9-gene biosynthetic gene cluster spt. Critical to salinipostin assembly is the {gamma}-butyrolactone synthase encoded by spt9. Here, we report the global distribution of spt9 among sequenced bacterial genomes, revealing a surprising diversity of gene homologs across 12 bacterial phyla, the majority of which are not known to produce {gamma}-butyrolactones. Further analyses uncovered a large group of spt-like gene clusters outside of the genus Salinispora, suggesting the production of new salinipostin-like diversity. These gene clusters show evidence of horizontal transfer between many bacterial taxa and location specific homologous recombination exchange among Salinispora strains. The results suggest that {gamma}-butyrolactone production may be more widespread than previously recognized. The identification of new {gamma}-butyrolactone biosynthetic gene clusters is the first step towards understanding the regulatory roles of the encoded small molecules in Actinobacteria. ImportanceSignaling molecules orchestrate a wide variety of bacterial behaviors. Among Actinobacteria, {gamma}-butyrolactones mediate morphological changes and regulate specialized metabolism. Despite their importance, few {gamma}-butyrolactones have been linked to their cognate biosynthetic gene clusters. A new series of {gamma}-butyrolactones called the salinipostins was recently identified from the marine actinomycete genus Salinispora and linked to the spt biosynthetic gene cluster. Here we report the detection of spt-like gene clusters in diverse bacterial families not known for the production of this class of compounds. This finding expands the taxonomic range of bacteria that may employ this class of compounds and provides opportunities to discover new compounds associated with chemical communication.

microbiology↗

Expansion of gamma-butyrolactone signaling molecule biosynthesis to phosphotriester natural products

Bacterial hormones, such as the iconic gamma-butyrolactone A-factor, are essential signaling molecules that regulate diverse physiological processes, including specialized metabolism. These low molecular weight compounds are common in Streptomyces species and display species-specific structural differences. Recently, unusual gamma-butyrolactone natural products called salinipostins were isolated from the marine actinomycete genus Salinispora based on their anti-malarial properties. As the salinipostins possess a rare phosphotriester motif of unknown biosynthetic origin, we set out to explore its construction by the widely conserved 9-gene spt operon in Salinispora species. We show through a series of in vivo and in vitro studies that the spt gene cluster dually encodes the saliniphostins and newly identified A-factor-like gamma-butyrolactones (Sal-GBLs). Remarkably, homologous biosynthetic gene clusters are widely distributed amongst many actinomycete genera, including Streptomyces, suggesting the significance of this operon in bacteria.

biochemistry↗