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

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 met...

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Autores principales: Gomes, Sofia I. F., Kielak, Anna M., Hannula, S. Emilia, Heinen, Robin, Jongen, Renske, Keesmaat, Ivor, De Long, Jonathan R., Bezemer, T. Martijn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807420/
https://www.ncbi.nlm.nih.gov/pubmed/33499994
http://dx.doi.org/10.1186/s42523-020-00055-3
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author Gomes, Sofia I. F.
Kielak, Anna M.
Hannula, S. Emilia
Heinen, Robin
Jongen, Renske
Keesmaat, Ivor
De Long, Jonathan R.
Bezemer, T. Martijn
author_facet Gomes, Sofia I. F.
Kielak, Anna M.
Hannula, S. Emilia
Heinen, Robin
Jongen, Renske
Keesmaat, Ivor
De Long, Jonathan R.
Bezemer, T. Martijn
author_sort Gomes, Sofia I. F.
collection PubMed
description 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.
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spelling pubmed-78074202021-01-19 Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities Gomes, Sofia I. F. Kielak, Anna M. Hannula, S. Emilia Heinen, Robin Jongen, Renske Keesmaat, Ivor De Long, Jonathan R. Bezemer, T. Martijn Anim Microbiome Research Article 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. BioMed Central 2020-10-07 /pmc/articles/PMC7807420/ /pubmed/33499994 http://dx.doi.org/10.1186/s42523-020-00055-3 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Gomes, Sofia I. F.
Kielak, Anna M.
Hannula, S. Emilia
Heinen, Robin
Jongen, Renske
Keesmaat, Ivor
De Long, Jonathan R.
Bezemer, T. Martijn
Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807420/
https://www.ncbi.nlm.nih.gov/pubmed/33499994
http://dx.doi.org/10.1186/s42523-020-00055-3
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