Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment
Many phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction betw...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.715601/full |
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| author | Jürgen C. Wierz Paul Gaube Dagmar Klebsch Martin Kaltenpoth Martin Kaltenpoth Laura V. Flórez Laura V. Flórez |
| author_facet | Jürgen C. Wierz Paul Gaube Dagmar Klebsch Martin Kaltenpoth Martin Kaltenpoth Laura V. Flórez Laura V. Flórez |
| author_sort | Jürgen C. Wierz |
| collection | DOAJ |
| description | Many phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction between microbe, insect, and plant. Here, we focus on two bacterial symbionts of the darkling beetle Lagria villosa that belong to the genus Burkholderia; the culturable strain B. gladioli Lv-StA and the reduced-genome strain Burkholderia Lv-StB. The strains can be transmitted vertically and confer protection to the beetle’s eggs, but Lv-StA can also proliferate in plants, and both symbiont strains have presumably evolved from plant pathogens. Notably, little is known about the role of the environment for the transmission dynamics and the maintenance of the symbionts. Through manipulative assays, we demonstrate the transfer of the symbionts from the beetle to wheat, rice and soybean plants, as well as leaf litter. In addition, we confirm that aposymbiotic larvae can pick up Lv-StA from dry leaves and the symbiont can successfully establish in the beetle’s symbiotic organs. Also, we show that the presence of plants and soil in the environment improves symbiont maintenance. These results indicate that the symbionts of L. villosa beetles are still capable of interacting with plants despite signatures of genome erosion and suggest that a mixed-mode of bacterial transmission is likely key for the persistence of the symbiosis. |
| first_indexed | 2024-12-23T13:55:38Z |
| format | Article |
| id | doaj.art-3ac97e2250e54c6489cf40321aade0ff |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-23T13:55:38Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3ac97e2250e54c6489cf40321aade0ff2022-12-21T17:44:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.715601715601Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant EnvironmentJürgen C. Wierz0Paul Gaube1Dagmar Klebsch2Martin Kaltenpoth3Martin Kaltenpoth4Laura V. Flórez5Laura V. Flórez6Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Mainz, GermanyMolecular Biodiversity Research Group, Center for Computational and Theoretical Biology, Julius Maximilian University of Würzburg, Würzburg, GermanyDepartment of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Mainz, GermanyDepartment of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Mainz, GermanyDepartment of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, GermanyDepartment of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Mainz, GermanyDepartment of Plant and Environmental Sciences, Section for Organismal Biology, University of Copenhagen, Copenhagen, DenmarkMany phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction between microbe, insect, and plant. Here, we focus on two bacterial symbionts of the darkling beetle Lagria villosa that belong to the genus Burkholderia; the culturable strain B. gladioli Lv-StA and the reduced-genome strain Burkholderia Lv-StB. The strains can be transmitted vertically and confer protection to the beetle’s eggs, but Lv-StA can also proliferate in plants, and both symbiont strains have presumably evolved from plant pathogens. Notably, little is known about the role of the environment for the transmission dynamics and the maintenance of the symbionts. Through manipulative assays, we demonstrate the transfer of the symbionts from the beetle to wheat, rice and soybean plants, as well as leaf litter. In addition, we confirm that aposymbiotic larvae can pick up Lv-StA from dry leaves and the symbiont can successfully establish in the beetle’s symbiotic organs. Also, we show that the presence of plants and soil in the environment improves symbiont maintenance. These results indicate that the symbionts of L. villosa beetles are still capable of interacting with plants despite signatures of genome erosion and suggest that a mixed-mode of bacterial transmission is likely key for the persistence of the symbiosis.https://www.frontiersin.org/articles/10.3389/fmicb.2021.715601/fullinsect symbiosismixed-mode transmissionBurkholderiaLagriinaeenvironmental symbiont acquisitionColeoptera |
| spellingShingle | Jürgen C. Wierz Paul Gaube Dagmar Klebsch Martin Kaltenpoth Martin Kaltenpoth Laura V. Flórez Laura V. Flórez Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment Frontiers in Microbiology insect symbiosis mixed-mode transmission Burkholderia Lagriinae environmental symbiont acquisition Coleoptera |
| title | Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment |
| title_full | Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment |
| title_fullStr | Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment |
| title_full_unstemmed | Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment |
| title_short | Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment |
| title_sort | transmission of bacterial symbionts with and without genome erosion between a beetle host and the plant environment |
| topic | insect symbiosis mixed-mode transmission Burkholderia Lagriinae environmental symbiont acquisition Coleoptera |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.715601/full |
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