Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities
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...
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| Format: | Article |
| Language: | English |
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BMC
2020-10-01
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| Series: | Animal Microbiome |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s42523-020-00055-3 |
| _version_ | 1818218676565835776 |
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| author | Sofia I. F. Gomes Anna M. Kielak S. Emilia Hannula Robin Heinen Renske Jongen Ivor Keesmaat Jonathan R. De Long T. Martijn Bezemer |
| author_facet | Sofia I. F. Gomes Anna M. Kielak S. Emilia Hannula Robin Heinen Renske Jongen Ivor Keesmaat Jonathan R. De Long T. Martijn Bezemer |
| author_sort | Sofia I. F. Gomes |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-12T07:27:33Z |
| format | Article |
| id | doaj.art-045d86884cc94c7ab892d281931cebf0 |
| institution | Directory Open Access Journal |
| issn | 2524-4671 |
| language | English |
| last_indexed | 2024-12-12T07:27:33Z |
| publishDate | 2020-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Animal Microbiome |
| spelling | doaj.art-045d86884cc94c7ab892d281931cebf02022-12-22T00:33:06ZengBMCAnimal Microbiome2524-46712020-10-012111210.1186/s42523-020-00055-3Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communitiesSofia I. F. Gomes0Anna M. Kielak1S. Emilia Hannula2Robin Heinen3Renske Jongen4Ivor Keesmaat5Jonathan R. De Long6T. Martijn Bezemer7Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW)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.http://link.springer.com/article/10.1186/s42523-020-00055-3InsectsLepidopteraRalstoniaSoilTyria jacobaeaeJacobaea vulgaris |
| spellingShingle | Sofia I. F. Gomes Anna M. Kielak S. Emilia Hannula Robin Heinen Renske Jongen Ivor Keesmaat Jonathan R. De Long T. Martijn Bezemer Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities Animal Microbiome Insects Lepidoptera Ralstonia Soil Tyria jacobaeae Jacobaea vulgaris |
| title | Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| title_full | Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| title_fullStr | Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| title_full_unstemmed | Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| title_short | Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| title_sort | microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities |
| topic | Insects Lepidoptera Ralstonia Soil Tyria jacobaeae Jacobaea vulgaris |
| url | http://link.springer.com/article/10.1186/s42523-020-00055-3 |
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