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Antibiotic-Producing Beneficial Bacteria in the Gut of the Burying Beetle Nicrophorus vespilloides.

ABSTRACT: The increasing prevalence of antibiotic-resistant human pathogens is a growing public concern and there is intense pressure to identify new antibacterial compounds that can be developed into antibiotics with novel mode of action. Evolutionary theory predicts that insects that have evolved to occupy sophisticated ecological niches by feeding and reproducing on carcasses will depend on their gut microbiome to prevent colonization by invading pathogens taken up with the diet. This inspired our hypothesis that the complex interactions between the core microbiome and the more flexible microbial communities dependent on the environment may promote the outsourcing of antibiotic synthesis to beneficial microbes. We tested this hypothesis by cultivating and characterizing bacteria isolated from the gut of the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses buried in the soil to avoid competitors such as fly maggots. The extracts of isolated bacteria were screened for activity against human pathogens such as Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Candida albicans. More than 400 strains were isolated, among which the crude extract of Serratia marcescens 2MH3-2 displayed promising activity against Staphylococcus aureus. Bioactivity-guided fractionation enabled purification of the primary antimicrobial compound of the extract. By LC-MS and NMR experiments, it was identified as serrawettin W2 (C38H61N5O9), the antibacterial and nematostatic activity of which was corroborated in our study. We postulate that this antibiotic could contribute to the control of both bacteria and phoretic nematodes in the gut, which compete for food when transferred to the carcass. Our study shows that the gut microbiome of N. vespilloides is a promising resource for the screening of antibiotic-producing bacteria.

SUBMITTER: Heise P

PROVIDER: S-EPMC6563848 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Antibiotic-Producing Beneficial Bacteria in the Gut of the Burying Beetle <i>Nicrophorus vespilloides</i>.

Heise Philipp P Liu Yang Y Degenkolb Thomas T Vogel Heiko H Schäberle Till F TF Vilcinskas Andreas A

Frontiers in microbiology 20190531

The increasing prevalence of antibiotic-resistant human pathogens is a growing public concern and there is intense pressure to identify new antibacterial compounds that can be developed into antibiotics with novel mode of action. Evolutionary theory predicts that insects that have evolved to occupy sophisticated ecological niches by feeding and reproducing on carcasses will depend on their gut microbiome to prevent colonization by invading pathogens taken up with the diet. This inspired our hypo ...[more]

PMID: 31244787

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Project description:Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.

Project description:Nicrophorus vespilloides is a social beetle that rears its offspring on decomposing carrion. Wild beetles are frequently associated with two types of macrobial symbionts, mites, and nematodes. Although these organisms are believed to be phoretic commensals that harmlessly use beetles as a means of transfer between carcasses, the role of these symbionts on N. vespilloides fitness is poorly understood. Here, we show that nematodes have significant negative effects on beetle fitness across a range of worm densities and also quantify the density-dependent transmission of worms between mating individuals and from parents to offspring. Using field-caught beetles, we provide the first report of a new nematode symbiont in N. vespilloides, most closely related to Rhabditoides regina, and show that worm densities are highly variable across individuals isolated from nature but do not differ between males and females. Next, by inoculating mating females with increasing densities of nematodes, we show that worm infections significantly reduce brood size, larval survival, and larval mass, and also eliminate the trade-off between brood size and larval mass. Finally, we show that nematodes are efficiently transmitted between mating individuals and from mothers to larvae, directly and indirectly via the carcass, and that worms persist through pupation. These results show that the phoretic nematode R. regina can be highly parasitic to burying beetles but can nevertheless persist because of efficient mechanisms of intersexual and intergenerational transmission. Phoretic species are exceptionally common and may cause significant harm to their hosts, even though they rely on these larger species for transmission to new resources. However, this harm may be inevitable and unavoidable if transmission of phoretic symbionts requires nematode proliferation. It will be important to determine the generality of our results for other phoretic associates of animals. It will equally be important to assess the fitness effects of phoretic species under changing resource conditions and in the field where diverse interspecific interactions may exacerbate or reduce the negative effects of phoresy.

Dataset Information

Antibiotic-Producing Beneficial Bacteria in the Gut of the Burying Beetle Nicrophorus vespilloides.

Publications

Antibiotic-Producing Beneficial Bacteria in the Gut of the Burying Beetle <i>Nicrophorus vespilloides</i>.

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