Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microb

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RESEARCH ARTICLE

Animal Microbiome

Open Access

Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities Sofia I. F. Gomes1†, Anna M. Kielak1†, S. Emilia Hannula1, Robin Heinen1,2, Renske Jongen1, Ivor Keesmaat1, Jonathan R. De Long1,3 and T. Martijn Bezemer1,4*

Abstract Background: Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not well understood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake and pathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages of wild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studies have shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examine microbiomes of a monophagous caterpillar (Tyria jacobaeae) collected from their natural host plant (Jacobaea vulgaris) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands, and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneath each of the host plants from which the caterpillars were collected. Results: The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar’s microbiome. Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillar samples across the three habitats. There was one amplicon sequence variant belonging to the genus Ralstonia that represented on average 53% of total community composition across all caterpillars. On average, one quarter of the caterpillar microbiome was shared with the soil. Conclusions: We found that the monophagous caterpillars collected from fields located more than 100 km apart were all dominated by a single Ralstonia. The remainder of the bacterial communities that were present resembled the local microbial communities in the soil in which the host plant was growing. Our findings provide an example of a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundant bacteria characteristic of soil communities. Keywords: Insects, Lepidoptera, Ralstonia, Soil, Tyria jacobaeae, Jacobaea vulgaris, Insect populations * Correspondence: [email protected] † Sofia I. F. Gomes and Anna M. Kielak contributed equally to this work. 1 Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands 4 Institute of Biology, Section Plant Ecology and Phytochemistry, Leiden University, P.O. Box 9505, 2300 RA Leiden, The Netherlands Full list of author informati