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      A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by Actinobacteria

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          Abstract

          Soil microbes produce a diverse array of natural products, including volatile organic compounds (VOCs). Volatile compounds are important molecules in soil habitats, where they mediate interactions between bacteria, fungi, insects, plants, and animals. We measured the VOCs produced by a broad diversity of soil- and dust-dwelling Actinobacteria in vitro. We detected a total of 126 unique volatile compounds, and each strain produced a unique combination of VOCs. While some of the compounds were produced by many strains, most were strain specific. Importantly, VOC profiles were more similar between closely related strains, indicating that evolutionary and ecological processes generate predictable patterns of VOC production. Finally, we observed that actinobacterial VOCs had both stimulatory and inhibitory effects on the growth of bacteria that represent a plant-beneficial symbiont and a plant-pathogenic strain, information that may lead to the development of novel strategies for plant disease prevention.

          ABSTRACT

          Soil microbes produce an immense diversity of metabolites, including volatile organic compounds (VOCs), which can shape the structure and function of microbial communities. VOCs mediate a multitude of microbe-microbe interactions, including antagonism. Despite their importance, the diversity and functional relevance of most microbial volatiles remain uncharacterized. We assembled a taxonomically diverse collection of 48 Actinobacteria isolated from soil and airborne dust and surveyed the VOCs produced by these strains on two different medium types in vitro using gas chromatography-mass spectrometry (GC-MS). We detected 126 distinct VOCs and structurally identified approximately 20% of these compounds, which were predominately C 1 to C 5 hetero-VOCs, including (oxygenated) alcohols, ketones, esters, and nitrogen- and sulfur-containing compounds. Each strain produced a unique VOC profile. While the most common VOCs were likely by-products of primary metabolism, most of the VOCs were strain specific. We observed a strong taxonomic and phylogenetic signal for VOC profiles, suggesting their role in finer-scale patterns of ecological diversity. Finally, we investigated the functional potential of these VOCs by assessing their effects on growth rates of both pathogenic and nonpathogenic pseudomonad strains. We identified sets of VOCs that correlated with growth inhibition and stimulation, information that may facilitate the development of microbial VOC-based pathogen control strategies.

          IMPORTANCE Soil microbes produce a diverse array of natural products, including volatile organic compounds (VOCs). Volatile compounds are important molecules in soil habitats, where they mediate interactions between bacteria, fungi, insects, plants, and animals. We measured the VOCs produced by a broad diversity of soil- and dust-dwelling Actinobacteria in vitro. We detected a total of 126 unique volatile compounds, and each strain produced a unique combination of VOCs. While some of the compounds were produced by many strains, most were strain specific. Importantly, VOC profiles were more similar between closely related strains, indicating that evolutionary and ecological processes generate predictable patterns of VOC production. Finally, we observed that actinobacterial VOCs had both stimulatory and inhibitory effects on the growth of bacteria that represent a plant-beneficial symbiont and a plant-pathogenic strain, information that may lead to the development of novel strategies for plant disease prevention.

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          Most cited references 65

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          MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

          We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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            RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.

            RAxML-VI-HPC (randomized axelerated maximum likelihood for high performance computing) is a sequential and parallel program for inference of large phylogenies with maximum likelihood (ML). Low-level technical optimizations, a modification of the search algorithm, and the use of the GTR+CAT approximation as replacement for GTR+Gamma yield a program that is between 2.7 and 52 times faster than the previous version of RAxML. A large-scale performance comparison with GARLI, PHYML, IQPNNI and MrBayes on real data containing 1000 up to 6722 taxa shows that RAxML requires at least 5.6 times less main memory and yields better trees in similar times than the best competing program (GARLI) on datasets up to 2500 taxa. On datasets > or =4000 taxa it also runs 2-3 times faster than GARLI. RAxML has been parallelized with MPI to conduct parallel multiple bootstraps and inferences on distinct starting trees. The program has been used to compute ML trees on two of the largest alignments to date containing 25,057 (1463 bp) and 2182 (51,089 bp) taxa, respectively. icwww.epfl.ch/~stamatak
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              Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.

              The Ribosomal Database Project (RDP) Classifier, a naïve Bayesian classifier, can rapidly and accurately classify bacterial 16S rRNA sequences into the new higher-order taxonomy proposed in Bergey's Taxonomic Outline of the Prokaryotes (2nd ed., release 5.0, Springer-Verlag, New York, NY, 2004). It provides taxonomic assignments from domain to genus, with confidence estimates for each assignment. The majority of classifications (98%) were of high estimated confidence (> or = 95%) and high accuracy (98%). In addition to being tested with the corpus of 5,014 type strain sequences from Bergey's outline, the RDP Classifier was tested with a corpus of 23,095 rRNA sequences as assigned by the NCBI into their alternative higher-order taxonomy. The results from leave-one-out testing on both corpora show that the overall accuracies at all levels of confidence for near-full-length and 400-base segments were 89% or above down to the genus level, and the majority of the classification errors appear to be due to anomalies in the current taxonomies. For shorter rRNA segments, such as those that might be generated by pyrosequencing, the error rate varied greatly over the length of the 16S rRNA gene, with segments around the V2 and V4 variable regions giving the lowest error rates. The RDP Classifier is suitable both for the analysis of single rRNA sequences and for the analysis of libraries of thousands of sequences. Another related tool, RDP Library Compare, was developed to facilitate microbial-community comparison based on 16S rRNA gene sequence libraries. It combines the RDP Classifier with a statistical test to flag taxa differentially represented between samples. The RDP Classifier and RDP Library Compare are available online at http://rdp.cme.msu.edu/.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                5 March 2019
                Mar-Apr 2019
                : 4
                : 2
                Affiliations
                [a ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Boulder, Colorado, USA
                [b ]Institute of Arctic and Alpine Research, University of Colorado, Boulder, Boulder, Colorado, USA
                [c ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Boulder, Colorado, USA
                University of California, Irvine
                Author notes
                Address correspondence to Noah Fierer, Noah.Fierer@ 123456colorado.edu .
                [*]

                Present address: Mallory Choudoir, Indigo Ag, Boston, Massachusetts, USA.

                Citation Choudoir M, Rossabi S, Gebert M, Helmig D, Fierer N. 2019. A phylogenetic and functional perspective on volatile organic compound production by Actinobacteria. mSystems 4:e00295-18. https://doi.org/10.1128/mSystems.00295-18.

                Article
                mSystems00295-18
                10.1128/mSystems.00295-18
                6401417
                Copyright © 2019 Choudoir et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 9, Figures: 6, Tables: 1, Equations: 0, References: 70, Pages: 15, Words: 9749
                Product
                Funding
                Funded by: MoSTR | National Science Foundation (NSF), https://doi.org/10.13039/501100008982;
                Award ID: DEB 1556753
                Award Recipient :
                Categories
                Research Article
                Applied and Environmental Science
                Editor's Pick
                Custom metadata
                March/April 2019

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