Dataset Information

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 in the microbiome, especially given the maintenance of the large lga gene cluster despite ongoing genome reduction.IMPORTANCE Associations 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.

SUBMITTER: Waterworth SC

PROVIDER: S-EPMC7042692 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

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

Waterworth Samantha C SC Flórez Laura V LV Rees Evan R ER Hertweck Christian C Kaltenpoth Martin M Kwan Jason C JC

mBio 20200225 1

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 ...[more]

PMID: 32098813

Similar Datasets

Project description:A symbiotic lifestyle frequently results in genome reduction in bacteria; the isolation of small populations promotes genetic drift and the fixation of deletions and deleterious mutations over time. Transitions in lifestyle, including host restriction or adaptation to an intracellular habitat, are thought to precipitate a wave of sequence degradation events and consequent proliferation of pseudogenes. We describe here a verrucomicrobial symbiont of the tunicate Lissoclinum sp. that appears to be undergoing such a transition, with low coding density and many identifiable pseudogenes. However, despite the overall drive toward genome reduction, this symbiont maintains seven copies of a large polyketide synthase (PKS) pathway for the mandelalides (mnd), cytotoxic compounds that likely constitute a chemical defense for the host. There is evidence of ongoing degradation in a small number of these repeats-including variable borders, internal deletions, and single nucleotide polymorphisms (SNPs). However, the gene dosage of most of the pathway is increased at least 5-fold. Correspondingly, this single pathway accounts for 19% of the genome by length and 25.8% of the coding capacity. This increased gene dosage in the face of generalized sequence degradation and genome reduction suggests that mnd genes are under strong purifying selection and are important to the symbiotic relationship. IMPORTANCE Secondary metabolites, which are small-molecule organic compounds produced by living organisms, provide or inspire drugs for many different diseases. These natural products have evolved over millions of years to provide a survival benefit to the producing organism and often display potent biological activity with important therapeutic applications. For instance, defensive compounds in the environment may be cytotoxic to eukaryotic cells, a property exploitable for cancer treatment. Here, we describe the genome of an uncultured symbiotic bacterium that makes such a cytotoxic metabolite. This symbiont is losing genes that do not endow a selective advantage in a hospitable host environment. Secondary metabolism genes, however, are repeated multiple times in the genome, directly demonstrating their selective advantage. This finding shows the strength of selective forces in symbiotic relationships and suggests that uncultured bacteria in such relationships should be targeted for drug discovery efforts.

Project description:BackgroundGenomes of Methanosarcina spp. are among the largest archaeal genomes. One suggested reason for that is massive horizontal gene transfer (HGT) from bacteria. Genes of bacterial origin may be involved in the central metabolism and solute transport, in particular sugar synthesis, sulfur metabolism, phosphate metabolism, DNA repair, transport of small molecules etc. Horizontally transferred (HT) genes are considered to play the key role in the ability of Methanosarcina spp. to inhabit diverse environments. At the moment, genomes of three Methanosarcina spp. have been sequenced, and while these genomes vary in length and number of protein-coding genes, they all have been shown to accumulate HT genes. However, previous estimates had been made when fewer archaeal genomes were known. Moreover, several Methanosarcinaceae genomes from other genera have been sequenced recently. Here, we revise the census of genes of bacterial origin in Methanosarcinaceae.ResultsAbout 5% of Methanosarcina genes have been shown to be horizontally transferred from various bacterial groups to the last common ancestor either of Methanosarcinaceae, or Methanosarcina, or later in the evolution. Simulation of the composition of the NCBI protein non-redundant database for different years demonstrates that the estimates of the HGT rate have decreased drastically since 2002, the year of publication of the first Methanosarcina genome. The phylogenetic distribution of HT gene donors is non-uniform. Most HT genes were transferred from Firmicutes and Proteobacteria, while no HGT events from Actinobacteria to the common ancestor of Methanosarcinaceae were found. About 50% of HT genes are involved in metabolism. Horizontal transfer of transcription factors is not common, while 46% of horizontally transferred genes have demonstrated differential expression in a variety of conditions. HGT of complete operons is relatively infrequent and half of HT genes do not belong to operons.ConclusionsWhile genes of bacterial origin are still more frequent in Methanosarcinaceae than in other Archaea, most HGT events described earlier as Methanosarcina-specific seem to have occurred before the divergence of Methanosarcinaceae. Genes horizontally transferred from bacteria to archaea neither tend to be transferred with their regulators, nor in long operons.

Dataset Information

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

Publications

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

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets