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Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria.

ABSTRACT: Streptomycetes are sessile bacteria that produce metabolites that impact the behavior of microbial communities. Emerging studies have demonstrated that Streptomyces spores are distributed through various mechanisms, but it remains unclear how spores are transported to their preferred microenvironments, such as plant roots. Here, we show that Streptomyces spores are capable of utilizing the motility machinery of other soil bacteria. Motility assays and microscopy studies reveal that Streptomyces spores are transported to plant tissues by interacting directly with the flagella of both gram-positive and gram-negative bacteria. Genetics experiments demonstrate that this form of motility is facilitated by structural proteins on the spore coat. These results demonstrate that nonmotile bacteria are capable of utilizing the motility machinery of other microbes to complete necessary stages of their lifecycle.

SUBMITTER: Muok AR

PROVIDER: S-EPMC8397704 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria.

Muok Alise R AR Claessen Dennis D Briegel Ariane A

The ISME journal 20210315 9

Streptomycetes are sessile bacteria that produce metabolites that impact the behavior of microbial communities. Emerging studies have demonstrated that Streptomyces spores are distributed through various mechanisms, but it remains unclear how spores are transported to their preferred microenvironments, such as plant roots. Here, we show that Streptomyces spores are capable of utilizing the motility machinery of other soil bacteria. Motility assays and microscopy studies reveal that Streptomyces ...[more]

PMID: 33723381

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Project description:1. Two bacteria, a Bacillus sp. and a Nocardia sp. (strain Z1) were isolated from soil by enrichment with 0.1 percent (v/v) pyridine and grew rapidly on this compound as sole C, N and energy source. The monohydroxypyridines, tetrahydropyridine, piperidine and some other analogues were not utilized for growth or oxidized by washed suspensions of either bacterium. 2. Cell-free extracts were unable to metabolize pyridine even after supplementation with a variety of cofactors or protecting agents. Treatment of cells with toluene led to rapid loss of the ability to oxidize pyridine. 3. In the presence of 10mM-semicarbazide at pH 6.0, Nocardia Z1 accumulated a semialdehyde idenditied as its 2,4-dinitrophenylhydrazone by chromatography, mixed melting point, mass spectrometry and isotope trapping from [2,6(-14)C]pyridine as glutarate semialdehyde. 4. Extracts of this bacterium prepared from cells grown with pyridine or exposed to the gratuitous inducer 2-picoline, contained high activities of a specific glutarate semialdehyde dehydrogenase. 5. Cells grown with pyridine or glutarate also contained a glutaric dialdehyde dehydrogenase, an acyl-CoA synthetase and elevated amounts of isocitrate lyase but no glutaryl-CoA dehydrogenase. 6. Bacillus 4 accumulated in the presence of 10mM-semicarbazide several acidic carbonyl compounds from pyridine among which was succinate semialdehyde. Extracts of this bacillus after growth of the cells with pyridine contained an inducible succinate semialdehyde dehydrogenase in amounts at least 50-fold over those found in succinate-grown cells. 7. Two mutants of this bacillus, selected for their inability to grow on pyridine were deficient in succinate semialdehyde dehydrogenase. 8. In the presence of 0.2mM-KCN, washed suspensions of Bacillus 4 accumulated formate and possibly formamide from pyridine. The use of [14C]pyridine showed that formate was derived from C-2 of the pyridine ring. 9. The organism had a specific formamide amidohydrolase cleaving formamide quantitatively to formate and NH3. 10. Formate was further oxidized by the particle fraction. There was no soluble formate dehydrogenase in extracts.

Project description:A novel actinobacterium, designated strain SMC 277T, was isolated from the clay soil in paddy field of Chonburi Province, Thailand, and characterized using polyphasic taxonomy. Strain SMC 277T formed straight chains of nonmotile cylindrical spores with smooth surface developed on aerial mycelia. The typical chemotaxonomic properties of members of the genus Streptomyces were observed in strain SMC 277T, e.g., cell wall peptidoglycan, whole cell sugars, major menaquinones, cellular fatty acids, and polar lipids. Chemotaxonomic data combined with mycelium and spore morphologies supported the assignment of strain SMC 277T to the genus Streptomyces. The results of comparative analysis of the 16S rRNA gene sequences confirmed that strain SMC 277T represented a member of the genus Streptomyces. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain SMC 277T shared the highest sequence similarity with Streptomyces bambusae NBRC 110903T (98.8%). Genome sequencing revealed a genome size of 6.55 Mbp and a digital G+C content of 73.4 mol%. In addition to the differences in phenotypic characteristics (morphology and physiology), values of ANI (ANIb and ANIm), AAI and dDDH between strain SMC 277T and its closest relative S. bambusae NBRC 110903T were 81.84, 86.77, 76.91 and 26.1%, respectively. Genome annotation and secondary metabolite gene cluster analysis predicted that SMC 277T contained 35 biosynthetic gene clusters encoding diverse bioactive secondary metabolites. It is in agreement with observed antimicrobial activity against drug-resistant bacteria associated with nosocomial infections (methicillin-resistant Staphylococcus aureus, extended-spectrum β-lactamase producing Klebsiella pneumoniae, and multidrug-resistant Acinetobacter baumannii). On the basis of these genotypic and phenotypic characteristics, strain SMC 277T can be characterized to represent a novel species of the genus Streptomyces, for which the name Streptomyces antimicrobicus is proposed. The type strain is SMC 277T (= TBRC 15568T = NBRC 115422T).

Dataset Information

Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria.

Publications

Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria.

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