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Title: Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome

Abstract

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 beetleLagria villosa, consisting of multiple bacterial symbionts related toBurkholderia 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 lagriamidelgabiosynthetic 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, especiallymore » given the maintenance of the largelgagene cluster despite ongoing genome reduction. IMPORTANCEAssociations between microorganisms and an animal, plant, or fungal host can result in increased dependence over time. This process is due partly to the bacterium not needing to produce nutrients that the host provides, leading to loss of genes that it would need to live independently and to a consequent reduction in genome size. It is often thought that genome reduction is aided by genetic isolation—bacteria that live in monocultures in special host organs, or inside host cells, have less access to other bacterial species from which they can obtain genes. Here, we describe exposure of a genome-reduced beetle symbiont to a community of related bacteria with nonreduced genomes. We show that the symbiont has acquired genes from other bacteria despite going through genome reduction, suggesting that isolation has not yet played a major role in this case of genome reduction, with horizontal gene gains still offering a potential route for adaptation.« less

Authors:
 [1];  [2];  [1];  [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Wisconsin, Madison, WI (United States). School of Pharmacy. Division of Pharmaceutical Sciences
  2. Johannes Gutenberg Univ., Mainz (Germany). Inst. of Organismic and Molecular Evolution. Dept. of Evolutionary Ecology
  3. 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
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. https://doi.org/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 = {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 beetleLagria villosa, consisting of multiple bacterial symbionts related toBurkholderia 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 lagriamidelgabiosynthetic 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 largelgagene cluster despite ongoing genome reduction. IMPORTANCEAssociations between microorganisms and an animal, plant, or fungal host can result in increased dependence over time. This process is due partly to the bacterium not needing to produce nutrients that the host provides, leading to loss of genes that it would need to live independently and to a consequent reduction in genome size. It is often thought that genome reduction is aided by genetic isolation—bacteria that live in monocultures in special host organs, or inside host cells, have less access to other bacterial species from which they can obtain genes. Here, we describe exposure of a genome-reduced beetle symbiont to a community of related bacteria with nonreduced genomes. We show that the symbiont has acquired genes from other bacteria despite going through genome reduction, suggesting that isolation has not yet played a major role in this case of genome reduction, with horizontal gene gains still offering a potential route for adaptation.},
doi = {10.1128/mbio.02430-19},
journal = {mBio (Online)},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {2}
}

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journal, February 2018

  • Goodall, Emily C. A.; Robinson, Ashley; Johnston, Iain G.
  • mBio, Vol. 9, Issue 1
  • DOI: 10.1128/mBio.02096-17

Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont
journal, November 2016

  • Powell, J. Elijah; Leonard, Sean P.; Kwong, Waldan K.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
  • DOI: 10.1073/pnas.1610856113

Symbiont-Supplemented Maternal Investment Underpinning Host’s Ecological Adaptation
journal, October 2014


IS26-Mediated Formation of Transposons Carrying Antibiotic Resistance Genes
journal, April 2016


An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles
journal, June 2018


Lateral gene transfer, bacterial genome evolution, and the Anthropocene: Lateral gene transfer in the Anthropocene
journal, October 2016

  • Gillings, Michael R.
  • Annals of the New York Academy of Sciences, Vol. 1389, Issue 1
  • DOI: 10.1111/nyas.13213

A Benchmark of Parametric Methods for Horizontal Transfers Detection
journal, April 2010


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0