Abstract
BackgroundInsect-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.ResultsThe 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.ConclusionsWe 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.
Highlights
Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly
Microbial diversity We found 3080 (335,283 reads) bacterial ASVs unique to caterpillar and 9594 (1,136,338 reads) ASVs unique to soil samples out of the total 11,658 highly abundant ASVs (> 0.1% relative abundance in each dataset)
Soil rarefaction curves did not reach a plateau and estimated diversity indices were often greater than observed values (SI Figure S4 and SI Table S2), suggesting that we failed to obtain a complete representation of the soil bacteria
Summary
Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. Interactions between insects and their associated bacterial communities range from mutualistic to pathogenic. A few of these symbiotic interactions have been intensively studied [3], suggesting that symbiotic microbiota provide nutrients and improve insect digestion [4, 5]. The low degree of morphological specialization in the gut and the rapid transit of food through the digestive tracks of caterpillars suggest a minor role for the microbial communities in their physiology [7]. These opposite trends emphasize the need to examine caterpillar-associated microbial communities. Most of our understanding of caterpillar microbiomes stems from caterpillars cultured under laboratory conditions and there is a dearth of studies that examine caterpillar-microbe interactions in their natural habitats
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