Lipopeptide-mediated bacterial interaction enables cooperative predator defense

Zhang, Shuaibing; Mukherji, Ruchira; Chowdhury, Somak; Reimer, L. M.; Stallforth, Pierre

doi:10.1073/pnas.2013759118

Cited by 30 publications

(29 citation statements)

References 47 publications

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“…Even so, all fungi, including Mortierella species, are threatened by micropredators such as nematodes ( 13 – 15 ). In order to oppose these predators, fungi have developed a diverse set of defense strategies.…”

mentioning

confidence: 99%

Bacterial endosymbionts protect beneficial soil fungus from nematode attack

Büttner

Niehs

Vandelannoote

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Fungi of the genus Mortierella occur ubiquitously in soils where they play pivotal roles in carbon cycling, xenobiont degradation, and promoting plant growth. These important fungi are, however, threatened by micropredators such as fungivorous nematodes, and yet little is known about their protective tactics. We report that Mortierella verticillata NRRL 6337 harbors a bacterial endosymbiont that efficiently shields its host from nematode attacks with anthelmintic metabolites. Microscopic investigation and 16S ribosomal DNA analysis revealed that a previously overlooked bacterial symbiont belonging to the genus Mycoavidus dwells in M. verticillata hyphae. Metabolic profiling of the wild-type fungus and a symbiont-free strain obtained by antibiotic treatment as well as genome analyses revealed that highly cytotoxic macrolactones (CJ-12,950 and CJ-13,357, syn. necroxime C and D), initially thought to be metabolites of the soil-inhabiting fungus, are actually biosynthesized by the endosymbiont. According to comparative genomics, the symbiont belongs to a new species (Candidatus Mycoavidus necroximicus) with 12% of its 2.2 Mb genome dedicated to natural product biosynthesis, including the modular polyketide-nonribosomal peptide synthetase for necroxime assembly. Using Caenorhabditis elegans and the fungivorous nematode Aphelenchus avenae as test strains, we show that necroximes exert highly potent anthelmintic activities. Effective host protection was demonstrated in cocultures of nematodes with symbiotic and chemically complemented aposymbiotic fungal strains. Image analysis and mathematical quantification of nematode movement enabled evaluation of the potency. Our work describes a relevant role for endofungal bacteria in protecting fungi against mycophagous nematodes.

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mentioning

confidence: 99%

Bacterial endosymbionts protect beneficial soil fungus from nematode attack

Büttner

Niehs

Vandelannoote

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…This structural composition provides lipopeptides with amphiphilic properties that confer versatile functionalities. Lipopeptides fulfill diverse ecological roles [e.g., as biosurfactants, in biofilm formation, and to access nutrients ( 4 , 5 ) and as mediators of interspecies interactions that include defense against predators, competition, pathogenicity, and symbiosis ( 1 , 6 , 7 )]. Relevant examples are the surfactin-type biosurfactants, orfamides and fengycins that induce systemic resistance in plants, and the antifungal echinocandins ( 1 , 3 , 8 , 9 ).…”

mentioning

confidence: 99%

Ribosomally derived lipopeptides containing distinct fatty acyl moieties

Hubrich

Bösch

Chepkirui

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Lipopeptides represent a large group of microbial natural products that include important antibacterial and antifungal drugs and some of the most-powerful known biosurfactants. The vast majority of lipopeptides comprise cyclic peptide backbones N-terminally equipped with various fatty acyl moieties. The known compounds of this type are biosynthesized by nonribosomal peptide synthetases, giant enzyme complexes that assemble their products in a non–gene-encoded manner. Here, we report the genome-guided discovery of ribosomally derived, fatty-acylated lipopeptides, termed selidamides. Heterologous reconstitution of three pathways, two from cyanobacteria and one from an arctic, ocean-derived alphaproteobacterium, allowed structural characterization of the probable natural products and suggest that selidamides are widespread over various bacterial phyla. The identified representatives feature cyclic peptide moieties and fatty acyl units attached to (hydroxy)ornithine or lysine side chains by maturases of the GCN5-related N-acetyltransferase superfamily. In contrast to nonribosomal lipopeptides that are usually produced as congener mixtures, the three selidamides are selectively fatty acylated with C10, C12, or C16 fatty acids, respectively. These results highlight the ability of ribosomal pathways to emulate products with diverse, nonribosomal-like features and add to the biocatalytic toolbox for peptide drug improvement and targeted discovery.

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“…Lipopeptides are amphipathic molecules which can act as biosurfactants, assisting Pseudomonas motility and colonization of their environmental niche. In addition, many of these molecules are also antibacterial, antifungal and antiprotozoal and have been shown to contribute to the biocontrol activity of plant growth promoting strains, as well as participate in cooperative predator defence, among many other activities [ 333 , 351 , 352 , 353 ]. As more strains are isolated, sequenced and their metabolomes assessed, more of these molecules are discovered [ 354 , 355 , 356 ].…”

Section: Pseudomonasmentioning

confidence: 99%

Beyond Soil-Dwelling Actinobacteria: Fantastic Antibiotics and Where to Find Them

Santos‐Aberturas

Vior

2022

Antibiotics

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Bacterial secondary metabolites represent an invaluable source of bioactive molecules for the pharmaceutical and agrochemical industries. Although screening campaigns for the discovery of new compounds have traditionally been strongly biased towards the study of soil-dwelling Actinobacteria, the current antibiotic resistance and discovery crisis has brought a considerable amount of attention to the study of previously neglected bacterial sources of secondary metabolites. The development and application of new screening, sequencing, genetic manipulation, cultivation and bioinformatic techniques have revealed several other groups of bacteria as producers of striking chemical novelty. Biosynthetic machineries evolved from independent taxonomic origins and under completely different ecological requirements and selective pressures are responsible for these structural innovations. In this review, we summarize the most important discoveries related to secondary metabolites from alternative bacterial sources, trying to provide the reader with a broad perspective on how technical novelties have facilitated the access to the bacterial metabolic dark matter.

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Lipopeptide-mediated bacterial interaction enables cooperative predator defense

Cited by 30 publications

References 47 publications

Bacterial endosymbionts protect beneficial soil fungus from nematode attack

Bacterial endosymbionts protect beneficial soil fungus from nematode attack

Ribosomally derived lipopeptides containing distinct fatty acyl moieties

Beyond Soil-Dwelling Actinobacteria: Fantastic Antibiotics and Where to Find Them

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