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Bacterivorous nematodes decipher microbial iron siderophores as prey cue in predator-prey interactions.

ABSTRACT: The minimal levels of biological-available iron in the environment impose growth limitation on all living organisms. Microbes often secrete high iron-binding-affinity siderophores at high concentrations for scavenging iron from the iron-limited habitats. However, the high prevalence of siderophores released by bacteria into the environment raises an intriguing question whether this chemical cue can be detected by bacterivorous predators. Here, we show that the bacterivorous Caenorhabditis elegans nematode could employ its chemosensory receptor Odr-10 to detect pyoverdine, an iron siderophore secreted by an environmental bacterium, Pseudomonas aeruginosa. This enabled the nematode predator to migrate toward the prey. Our soil microcosm study showed that the detection of pyoverdine and subsequent feeding of P. aeruginosa prey by C. elegans could lead to the expansion of its population. These results showed that siderophores are a prey chemical cue by predators, with key implications in predator-prey interactions.

SUBMITTER: Hu M

PROVIDER: S-EPMC10801909 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Bacterivorous nematodes decipher microbial iron siderophores as prey cue in predator-prey interactions.

Hu Minqi M Ma Yeping Y Chua Song Lin SL

Proceedings of the National Academy of Sciences of the United States of America 20240108 3

The minimal levels of biological-available iron in the environment impose growth limitation on all living organisms. Microbes often secrete high iron-binding-affinity siderophores at high concentrations for scavenging iron from the iron-limited habitats. However, the high prevalence of siderophores released by bacteria into the environment raises an intriguing question whether this chemical cue can be detected by bacterivorous predators. Here, we show that the bacterivorous <i>Caenorhabditis ele ...[more]

PMID: 38190542

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Project description:Microbial symbiosis drives physiological processes of higher-order systems, including the acquisition and consumption of nutrients that support symbiotic partner reproduction. Metabolic analytics provide new avenues to examine how chemical ecology, or the conversion of existing biomass to new forms, changes over a symbiotic life cycle. We applied these approaches to the nematode Steinernema carpocapsae, its mutualist bacterium, Xenorhabdus nematophila, and the insects they infect. The nematode-bacterium pair infects, kills, and reproduces in an insect until nutrients are depleted. To understand the conversion of insect biomass over time into either nematode or bacterium biomass, we integrated information from trophic, metabolomic, and gene regulation analyses. Trophic analysis established bacteria as meso-predators and primary insect consumers. Nematodes hold a trophic position of 4.6, indicative of an apex predator, consuming bacteria and likely other nematodes. Metabolic changes associated with Galleria mellonella insect bioconversion were assessed using multivariate statistical analyses of metabolomics data sets derived from sampling over an infection time course. Statistically significant, discrete phases were detected, indicating the insect chemical environment changes reproducibly during bioconversion. A novel hierarchical clustering method was designed to probe molecular abundance fluctuation patterns over time, revealing distinct metabolite clusters that exhibit similar abundance shifts across the time course. Composite data suggest bacterial tryptophan and nematode kynurenine pathways are coordinated for reciprocal exchange of tryptophan and NAD+ and for synthesis of intermediates that can have complex effects on bacterial phenotypes and nematode behaviors. Our analysis of pathways and metabolites reveals the chemistry underlying the recycling of organic material during carnivory. IMPORTANCE The processes by which organic life is consumed and reborn in a complex ecosystem were investigated through a multiomics approach applied to the tripartite Xenorhabdus bacterium-Steinernema nematode-Galleria insect symbiosis. Trophic analyses demonstrate the primary consumers of the insect are the bacteria, and the nematode in turn consumes the bacteria. This suggests the Steinernema-Xenorhabdus mutualism is a form of agriculture in which the nematode cultivates the bacterial food sources by inoculating them into insect hosts. Metabolomics analysis revealed a shift in biological material throughout progression of the life cycle: active infection, insect death, and conversion of cadaver tissues into bacterial biomass and nematode tissue. We show that each phase of the life cycle is metabolically distinct, with significant differences including those in the tricarboxylic acid cycle and amino acid pathways. Our findings demonstrate that symbiotic life cycles can be defined by reproducible stage-specific chemical signatures, enhancing our broad understanding of metabolic processes that underpin a three-way symbiosis.

Dataset Information

Bacterivorous nematodes decipher microbial iron siderophores as prey cue in predator-prey interactions.

Publications

Bacterivorous nematodes decipher microbial iron siderophores as prey cue in predator-prey interactions.

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