Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome
Abstract
Symbiotic mutualisms of bacteria and animals are ubiquitous in nature, running a continuum from facultative to obligate from the perspectives of both partners. The loss of functions required for living independently but not within a host gives rise to reduced genomes in many symbionts. Although the phenomenon of genome reduction can be explained by existing evolutionary models, the initiation of the process is not well understood. Here, we describe the microbiome associated with the eggs of the beetle Lagria villosa, consisting of multiple bacterial symbionts related to Burkholderia gladioli, including a reduced-genome symbiont thought to be the exclusive producer of the defensive compound lagriamide. We show that the putative lagriamide-producing symbiont is the only member of the microbiome undergoing genome reduction and that it has already lost the majority of its primary metabolism and DNA repair pathways. The key step preceding genome reduction in the symbiont was likely the horizontal acquisition of the putative lagriamide lga biosynthetic gene cluster. Unexpectedly, we uncovered evidence of additional horizontal transfers to the symbiont’s genome while genome reduction was occurring and despite a current lack of genes needed for homologous recombination. These gene gains may have given the genome-reduced symbiont a selective advantage inmore »
- Authors:
-
[2];
[1]
- Univ. of Wisconsin, Madison, WI (United States). School of Pharmacy. Division of Pharmaceutical Sciences
- Johannes Gutenberg Univ., Mainz (Germany). Inst. of Organismic and Molecular Evolution. Dept. of Evolutionary Ecology
- Leibniz Inst. for Natural Products Research and Infection Biology, Jena (Germany); Friedrich Schiller Univ., Jena (Germany). Dept. of Natural Product Chemistry
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1626148
- Grant/Contract Number:
- FG02-04ER63917
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology; Burkholderia; insects; metagenomics; natural products; symbiosis
Citation Formats
Waterworth, Samantha C., Flórez, Laura V., Rees, Evan R., Hertweck, Christian, Kaltenpoth, Martin, and Kwan, Jason C. Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome. United States: N. p., 2020.
Web. doi:10.1128/mbio.02430-19.
Waterworth, Samantha C., Flórez, Laura V., Rees, Evan R., Hertweck, Christian, Kaltenpoth, Martin, & Kwan, Jason C. Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome. United States. https://doi.org/10.1128/mbio.02430-19
Waterworth, Samantha C., Flórez, Laura V., Rees, Evan R., Hertweck, Christian, Kaltenpoth, Martin, and Kwan, Jason C. Tue .
"Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome". United States. https://doi.org/10.1128/mbio.02430-19. https://www.osti.gov/servlets/purl/1626148.
@article{osti_1626148,
title = {Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome},
author = {Waterworth, Samantha C. and Flórez, Laura V. and Rees, Evan R. and Hertweck, Christian and Kaltenpoth, Martin and Kwan, Jason C.},
abstractNote = {Symbiotic mutualisms of bacteria and animals are ubiquitous in nature, running a continuum from facultative to obligate from the perspectives of both partners. The loss of functions required for living independently but not within a host gives rise to reduced genomes in many symbionts. Although the phenomenon of genome reduction can be explained by existing evolutionary models, the initiation of the process is not well understood. Here, we describe the microbiome associated with the eggs of the beetle Lagria villosa, consisting of multiple bacterial symbionts related to Burkholderia gladioli, including a reduced-genome symbiont thought to be the exclusive producer of the defensive compound lagriamide. We show that the putative lagriamide-producing symbiont is the only member of the microbiome undergoing genome reduction and that it has already lost the majority of its primary metabolism and DNA repair pathways. The key step preceding genome reduction in the symbiont was likely the horizontal acquisition of the putative lagriamide lga biosynthetic gene cluster. Unexpectedly, we uncovered evidence of additional horizontal transfers to the symbiont’s genome while genome reduction was occurring and despite a current lack of genes needed for homologous recombination. These gene gains may have given the genome-reduced symbiont a selective advantage in the microbiome, especially given the maintenance of the large lga gene cluster despite ongoing genome reduction.},
doi = {10.1128/mbio.02430-19},
journal = {mBio (Online)},
number = 1,
volume = 11,
place = {United States},
year = {Tue Feb 25 00:00:00 EST 2020},
month = {Tue Feb 25 00:00:00 EST 2020}
}
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