Dataset Information

Cascading effects on bacterial communities: cattle grazing causes a shift in the microbiome of a herbivorous caterpillar.

ABSTRACT: Large mammalian herbivores greatly influence the functioning of grassland ecosystems. Through plant consumption, excreta, and trampling, they modify biodiversity, nutrient cycling, and soil properties. Grazing mammals can also alter soil and rhizosphere bacterial communities, but their effect on the microbiome of other animals in the habitat (i.e., insects) is unknown. Using an experimental field approach and Illumina MiSeq 16S rRNA gene sequencing, we analyzed the influence of cattle grazing on the microbial community of spring webworm caterpillars, Ocnogyna loewii. Our experimental setup included replicated grazed and non-grazed paddocks from which caterpillars were collected twice (first-second and fourth-fifth instar). The caterpillars' microbiome is composed mostly of Proteobacteria and Firmicutes, and contains a potential symbiont from the genus Carnobacterium (55% of reads). We found that grazing significantly altered the microbiome composition of late instar caterpillars, probably through changes in diet (plant) composition and availability. Furthermore, the microbiome composition of early instar caterpillars significantly differed from late instar caterpillars in 221 OTUs (58 genera). Pseudomonas and Acinetobacter were dominant in early instars, while Carnobacterium and Acinetobacter were dominant in late instars. This study provides new ecological perspectives on the cascading effects mammalian herbivores may have on the microbiome of other animals in their shared habitat.

SUBMITTER: Berman TS

PROVIDER: S-EPMC6052054 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Cascading effects on bacterial communities: cattle grazing causes a shift in the microbiome of a herbivorous caterpillar.

Berman Tali S TS Laviad-Shitrit Sivan S Lalzar Maya M Halpern Malka M Inbar Moshe M

The ISME journal 20180425 8

Large mammalian herbivores greatly influence the functioning of grassland ecosystems. Through plant consumption, excreta, and trampling, they modify biodiversity, nutrient cycling, and soil properties. Grazing mammals can also alter soil and rhizosphere bacterial communities, but their effect on the microbiome of other animals in the habitat (i.e., insects) is unknown. Using an experimental field approach and Illumina MiSeq 16S rRNA gene sequencing, we analyzed the influence of cattle grazing on ...[more]

PMID: 29695861

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Project description:Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome.

Project description:BACKGROUND:House fly larvae (Musca domestica L.) require a live microbial community to successfully develop. Cattle manure is rich in organic matter and microorganisms, comprising a suitable substrate for larvae who feed on both the decomposing manure and the prokaryotic and eukaryotic microbes therein. Microbial communities change as manure ages, and when fly larvae are present changes attributable to larval grazing also occur. Here, we used high throughput sequencing of 16S and 18S rRNA genes to characterize microbial communities in dairy cattle manure and evaluated the changes in those communities over time by comparing the communities in fresh manure to aged manure with or without house fly larvae. RESULTS:Bacteria, archaea and protist community compositions significantly differed across manure types (e.g. fresh, aged, larval-grazed). Irrespective of manure type, microbial communities were dominated by the following phyla: Euryarchaeota (Archaea); Proteobacteria, Firmicutes and Bacteroidetes (Bacteria); Ciliophora, Metamonanda, Ochrophyta, Apicomplexa, Discoba, Lobosa and Cercozoa (Protists). Larval grazing significantly reduced the abundances of Bacteroidetes, Ciliophora, Cercozoa and increased the abundances of Apicomplexa and Discoba. Manure aging alone significantly altered the abundance bacteria (Acinetobacter, Clostridium, Petrimonas, Succinovibro), protists (Buxtonella, Enteromonas) and archaea (Methanosphaera and Methanomassiliicoccus). Larval grazing also altered the abundance of several bacterial genera (Pseudomonas, Bacteroides, Flavobacterium, Taibaiella, Sphingopyxis, Sphingobacterium), protists (Oxytricha, Cercomonas, Colpodella, Parabodo) and archaea (Methanobrevibacter and Methanocorpusculum). Overall, larval grazing significantly reduced bacterial and archaeal diversities but increased protist diversity. Moreover, total carbon (TC) and nitrogen (TN) decreased in larval grazed manure, and both TC and TN were highly correlated with several of bacterial, archaeal and protist communities. CONCLUSIONS:House fly larval grazing altered the abundance and diversity of bacterial, archaeal and protist communities differently than manure aging alone. Fly larvae likely alter community composition by directly feeding on and eliminating microbes and by competing with predatory microbes for available nutrients and microbial prey. Our results lend insight into the role house fly larvae play in shaping manure microbial communities and help identify microbes that house fly larvae utilize as food sources in manure. Information extrapolated from this study can be used to develop manure management strategies to interfere with house fly development and reduce house fly populations.

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Dataset Information

Cascading effects on bacterial communities: cattle grazing causes a shift in the microbiome of a herbivorous caterpillar.

Publications

Cascading effects on bacterial communities: cattle grazing causes a shift in the microbiome of a herbivorous caterpillar.

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