Dataset Information

Bacterial vitamin B₁₂ production enhances nematode predatory behavior.

ABSTRACT: Although the microbiota is known to affect host development, metabolism, and immunity, its impact on host behavior is only beginning to be understood. In order to better characterize behavior modulation by host-associated microorganisms, we investigated how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. This nematode is a predator that feeds on the larvae of other nematodes, including Caenorhabditis elegans. By growing P. pacificus on different bacteria and testing their ability to kill C. elegans, we reveal large differences in killing efficiencies, with a Novosphingobium species showing the strongest enhancement. This enhanced killing was not accompanied by an increase in feeding, which is a phenomenon known as surplus killing, whereby predators kill more prey than necessary for sustenance. Our RNA-seq data demonstrate widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated screening of bacterial mutants with altered transcriptional responses. We identified bacterial production of vitamin B₁₂ as an important cause of such enhanced predatory behavior. Although vitamin B₁₂ is an essential cofactor for detoxification and metabolite biosynthesis, shown previously to accelerate development in C. elegans, supplementation with this enzyme cofactor amplified surplus killing in P. pacificus, whereas mutants in vitamin B₁₂-dependent pathways reduced surplus killing. By demonstrating that production of vitamin B₁₂ by host-associated microbiota can affect complex host behaviors, we reveal new connections between animal diet, microbiota, and nervous system.

SUBMITTER: Akduman N

PROVIDER: S-EPMC7242318 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Bacterial vitamin B<sub>12</sub> production enhances nematode predatory behavior.

Akduman Nermin N Lightfoot James W JW Röseler Waltraud W Witte Hanh H Lo Wen-Sui WS Rödelsperger Christian C Sommer Ralf J RJ

The ISME journal 20200309 6

Although the microbiota is known to affect host development, metabolism, and immunity, its impact on host behavior is only beginning to be understood. In order to better characterize behavior modulation by host-associated microorganisms, we investigated how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. This nematode is a predator that feeds on the larvae of other nematodes, including Caenorhabditis elegans. By growing P. pacificus on different bacteri ...[more]

PMID: 32152389

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Project description:Bacterial hopanoid lipids are ubiquitous in the geologic record and serve as biomarkers for reconstructing Earth's climatic and biogeochemical evolution. Specifically, the abundance of 2-methylhopanoids deposited during Mesozoic ocean anoxic events (OAEs) and other intervals has been interpreted to reflect proliferation of nitrogen-fixing marine cyanobacteria. However, there currently is no conclusive evidence for 2-methylhopanoid production by extant marine cyanobacteria. As an alternative explanation, here we report 2-methylhopanoid production by bacteria of the genus Nitrobacter, cosmopolitan nitrite oxidizers that inhabit nutrient-rich freshwater, brackish, and marine environments. The model organism Nitrobacter vulgaris produced only trace amounts of 2-methylhopanoids when grown in minimal medium or with added methionine, the presumed biosynthetic methyl donor. Supplementation of cultures with cobalamin (vitamin B12) increased nitrite oxidation rates and stimulated a 33-fold increase of 2-methylhopanoid abundance, indicating that the biosynthetic reaction mechanism is cobalamin dependent. Because Nitrobacter spp. cannot synthesize cobalamin, we postulate that they acquire it from organisms inhabiting a shared ecological niche-for example, ammonia-oxidizing archaea. We propose that during nutrient-rich conditions, cobalamin-based mutualism intensifies upper water column nitrification, thus promoting 2-methylhopanoid deposition. In contrast, anoxia underlying oligotrophic surface ocean conditions in restricted basins would prompt shoaling of anaerobic ammonium oxidation, leading to low observed 2-methylhopanoid abundances. The first scenario is consistent with hypotheses of enhanced nutrient loading during OAEs, while the second is consistent with the sedimentary record of Pliocene-Pleistocene Mediterranean sapropel events. We thus hypothesize that nitrogen cycling in the Pliocene-Pleistocene Mediterranean resembled modern, highly stratified basins, whereas no modern analog exists for OAEs.

Project description:Vitamin B12 is synthesized only by certain bacteria and archaeon, but not by plants. The synthesized vitamin B12 is transferred and accumulates in animal tissues, which can occur in certain plant and mushroom species through microbial interaction. In particular, the meat and milk of herbivorous ruminant animals (e.g. cattle and sheep) are good sources of vitamin B12 for humans. Ruminants acquire vitamin B12, which is considered an essential nutrient, through a symbiotic relationship with the bacteria present in their stomachs. In aquatic environments, most phytoplankton acquire vitamin B12 through a symbiotic relationship with bacteria, and they become food for larval fish and bivalves. Edible plants and mushrooms rarely contain a considerable amount of vitamin B12, mainly due to concomitant bacteria in soil and/or their aerial surfaces. Thus, humans acquire vitamin B12 formed by microbial interaction via mainly ruminants and fish (or shellfish) as food sources. In this review, up-to-date information on vitamin B12 sources and bioavailability are also discussed. Impact statement To prevent vitamin B12 (B12) deﬁciency in high-risk populations such as vegetarians and elderly subjects, it is necessary to identify foods that contain high levels of B12. B12 is synthesized by only certain bacteria and archaeon, but not by plants or animals. The synthesized B12 is transferred and accumulated in animal tissues, even in certain plant tissues via microbial interaction. Meats and milks of herbivorous ruminant animals are good sources of B12 for humans. Ruminants acquire the essential B12 through a symbiotic relationship with bacteria inside the body. Thus, we also depend on B12-producing bacteria located in ruminant stomachs. While edible plants and mushrooms rarely contain a considerable amount of B12, mainly due to concomitant bacteria in soil and/or their aerial surfaces. In this mini-review, we described up-to-date information on B12 sources and bioavailability with reference to the interaction of microbes as B12-producers.

Dataset Information

Bacterial vitamin B₁₂ production enhances nematode predatory behavior.

Publications

Bacterial vitamin B<sub>12</sub> production enhances nematode predatory behavior.

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Dataset Information

Bacterial vitamin B12 production enhances nematode predatory behavior.

Publications

Bacterial vitamin B<sub>12</sub> production enhances nematode predatory behavior.

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OmicsDI is part of the ELIXIR infrastructure

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Bacterial vitamin B₁₂ production enhances nematode predatory behavior.