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Creamer, K. E.

Publications and source records attributed to Creamer, K. E..

4 recordsLinked to original sources

Microbial autotrophy is widespread across soils and most prevalent in deep and saturated environments

Genes for CO2 fixation occur in soil microorganisms, but little is known about the pathways that are most common across ecosystem types, the organisms with these genes, where different CO2 fixation pathways are most prevalent, and the energy sources that support autotrophy across ecosystems. Here, we investigated microbial capacity for autotrophy in soils using 853 metagenomes and 201 metatranscriptomes from a wide range of terrestrial ecosystems (agricultural soils, wetlands, weathering rock). Autotrophy-associated RuBisCO (Form I and II) is widely encoded across all soils and occurs in bacteria from numerous lineages (38 phyla). RuBisCO Form IE is consistently more phylogenetically diverse in soils than in marine ecosystems, suggesting that it may have evolved to function in soil-like environments. A newly discovered deeply branching Form I RuBisCO, Form I, supports the hypothesis that Form I RuBisCO originated in anaerobic environments. Further, saturated soils harbor more, and more distinct, autotrophic microbes, many of which may use the Calvin-Benson-Bassham cycle or Wood-Ljungdahl pathway for CO2 fixation. Overall, the results indicate that autotrophy is a particularly important metabolism in deep, saturated soils and weathering rock.

microbiology↗

Metagenomic Data Reveal Type I Polyketide Synthase Distributions Across Biomes

Microbial polyketide synthase (PKS) genes encode the biosynthesis of many biomedically important natural products, yet only a small fraction of natures polyketide biosynthetic potential has been realized. Much of this potential originates from type I PKSs (T1PKSs), which can be delineated into different classes and subclasses based on domain organization and structural features of the compounds encoded. Notably, phylogenetic relationships among PKS ketosynthase (KS) domains provide a method to classify the larger and more complex genes in which they occur. Increased access to large metagenomic datasets from diverse habitats provides opportunities to assess T1PKS biosynthetic diversity and distributions through the analysis of KS domain sequences. Here, we used the webtool NaPDoS2 to detect and classify over 35,000 type I KS domains from 137 metagenomic data sets reported from eight diverse biomes. We found biome-specific separation with soils enriched in modular cis-AT and hybrid cis-AT KSs relative to other biomes and marine sediments enriched in KSs associated with PUFA and enediyne biosynthesis. By extracting full-length KS domains, we linked the phylum Actinobacteria to soil-specific enediyne and cis-AT clades and identified enediyne and monomodular KSs in phyla from which the associated compound classes have not been reported. These sequences were phylogenetically distinct from those associated with experimentally characterized PKSs suggesting novel structures or enzyme functions remain to be discovered. Lastly, we employed our metagenome-extracted KS domains to evaluate commonly used type I KS PCR primers and identified modifications that could increase the KS sequence diversity recovered from amplicon libraries. ImportancePolyketides are a crucial source of medicines, agrichemicals, and other commercial products. Advances in our understanding of polyketide biosynthesis coupled with the accumulation of metagenomic sequence data provide new opportunities to assess polyketide biosynthetic potential across biomes. Here, we used the webtool NaPDoS2 to assess type I PKS diversity and distributions by detecting and classifying KS domains across 137 metagenomes. We show that biomes are differentially enriched in KS domain classes, providing a roadmap for future biodiscovery strategies. Further, KS phylogenies reveal both biome-specific clades that do not include biochemically characterized PKSs, highlighting the biosynthetic potential of poorly explored environments. The large metagenome-derived KS dataset allowed us to identify regions of commonly used type I KS PCR primers that could be modified to capture a larger extent of KS diversity. These results facilitate both the search for novel polyketides and our understanding of the biogeographical distribution of PKSs across earths major biomes.

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↗